Review Article The Increasing Interest of ANAMMOX...

Hindawi Publishing CorporationBioMed Research InternationalVolume 2013 Article ID 134914 21 pageshttpdxdoiorg1011552013134914

Review ArticleThe Increasing Interest of ANAMMOX Research in ChinaBacteria Process Development and Application

Mohammad Ali12 Li-Yuan Chai12 Chong-Jian Tang12 Ping Zheng3 Xiao-Bo Min12

Zhi-Hui Yang12 Lei Xiong12 and Yu-Xia Song12

1 Department of Environmental Engineering School of Metallurgy and Environment Central South UniversityLushan South Road 932 Changsha Hunan 410083 China

2National Engineering Research Centre for Control and Treatment of Heavy Metal Pollution Changsha 410083 China3Department of Environmental Engineering Zhejiang University Hangzhou 310058 China

Correspondence should be addressed to Chong-Jian Tang chjtangcsueducn

Received 20 September 2013 Accepted 19 October 2013

Academic Editor Qaisar Mahmood

Copyright copy 2013 Mohammad Ali et alThis is an open access article distributed under the Creative CommonsAttribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Nitrogen pollution created severe environmental problems and increasingly has become an important issue in China Since thefirst discovery of ANAMMOX in the early 1990s this related technology has become a promising as well as sustainable bioprocessfor treating strong nitrogenous wastewater Many Chinese research groups have concentrated their efforts on the ANAMMOXresearch including bacteria process development and application during the past 20 years A series of new and outstandingoutcomes including the discovery of new ANAMMOX bacterial species (Brocadia sinica) sulfate-dependent ANAMMOX bacteria(Anammoxoglobus sulfate and Bacillus benzoevorans) and the highest nitrogen removal performance (743ndash767 kg-Nm3d) in labscale granule-based UASB reactors around the world were achieved The characteristics structure packing pattern and floatationmechanism of the high-rate ANAMMOX granules in ANAMMOX reactors were also carefully illustrated by native researchersNowadays some pilot and full-scale ANAMMOX reactors were constructed to treat different types of ammonium-rich wastewaterincluding monosodium glutamate wastewater pharmaceutical wastewater and leachate The prime objective of the present reviewis to elucidate the ongoing ANAMMOX research in China from lab scale to full scale applications comparative analysis andevaluation of significant findings and to set a design to usher ANAMMOX research in culmination

1 Introduction

Anaerobic ammonia oxidation (ANAMMOX) process is anovel and promising biological nitrogen removal biotechnol-ogy that has been successfully applied from the beginning ofthis century [1ndash3] ANAMMOX bacteria convert ammoniumdirectly to nitrogen gas with nitrite as the electron acceptorunder anoxic conditions From the discovery of the ANAM-MOX process in mid 1990s [1] it has been regarded as a cost-effective and environment-friendly way to treat wastewatercontaining high ammonium concentrations [4]

By smart application of ANAMMOX in municipal treat-ment wastewater treatment plants could be converted fromenergy-consuming into energy-producing systems [5] Itbecomes a hot topic in the fields of microbiology andenvironmental science and engineering due to its merits

of effective removal of both ammonium and nitrite underanaerobic conditions with high removal rate little sludgeproduction and low operational cost [5ndash8]

The drawback of this new and cost-effective process is thelow growth rate of involved bacteria (00027 hminus1 reported byStrous et al [2] 0016 hminus1 reported by Isaka et al [9]) Sothe ANAMMOX reactors are often operated at a long solidsretention time (SRT) in order to accumulate the necessarybiomass in the system [2 10 11] Till now 5 genera of ANAM-MOX bacteria including 13 species [12] have been identifiedand among these Candidatus Brocadia sinica has beendiscovered in China [13] On the other hand the existence ofsulfate-dependent anaerobic ammonium oxidation has beenrecognized so far but the involved microorganisms havebeen isolated infrequently Recently new species of sulfate-dependent ANAMMOX bacteria Anammoxoglobus sulfate

2 BioMed Research International

[14] and Bacillus benzoevorans [15] have been discoveredin China which are the functional community to removeammonium and sulfate simultaneously

High rate is one of the prime objectives for ANAMMOXprocess Within the last decades some specialized reactorsystems such as sequencing batch reactor (SBR) [2 16ndash19] rotating biological contactor (RBC) [18] trickling filter[19] UBF reactor [20] granular sludge bed reactor [21]and membrane bioreactor [3 22] have been introduced inboth laboratory and full scale to obtain high removal rateand finally noticed that these reactors played an importantrole in securing high rate performance for ammonium andnitrite removal The NRR of conventional nitrogen removalbiotechnologies was less than 05 kg-Nm3d [20] while forANAMMOX process it was higher than 5 kg-Nm3d asobtained by a number of researchers using different reactorssuch as upflow biofilter upflow anaerobic sludge blanket(UASB) reactor and gas-lift reactor [3 23ndash26]

Nitrogen pollution (N-pollution) causes serious environ-mental problems N-pollution not only hampers the sustain-able development of agriculture fishery tourism and so forthbut also threatens the living environment of human beingsAccording to the report of ldquothe state of the environmentin China (2009)rdquo the ammonium emission was up to 123million tons per year [27] Thus it was necessary to removenitrogen from different ammonium wastewater in ChinaTo fulfill the demand the research groups in China startedto carry out ANAMMOX research and obtained significantoutcomes As a part of continuation of ANAMMOX researchnitrogen removal rate higher than 10 kg-Nm3dwas obtainedby a significant number of researchers in China [26 28ndash30] Till now the highest NRR in the world was reportedby Chinese research group which was 743ndash767 kg-Nm3dat hydraulic retention time (HRT) of 016 h [28] Besidesnitrogen sulfur is another necessary nutrient for all livingcreatures which means that no one can grow and reproducewithout them [31 32] Ammonium and sulfate are coexistentin seawater and sediments with the average concentrations of100mMand 20mM respectively and this coexistence offers abasic condition for sulfate-dependent anaerobic ammoniumoxidation [33] Using this basic condition simultaneousremoval of ammonium and sulfate was discovered in 2001in an anaerobic fluidized-bed reactor by Fdz-Polanco etal [34] and they reported that 80 sulfate was convertedto elemental sulfur accompanied by ammonium oxidationto dinitrogen gas Subsequently the existence of sulfate-dependent anaerobic ammonium oxidation has been con-firmed by other researchers [14 35ndash38] Sulfate-dependentANAMMOX process was also reported by a number ofresearchers in China [14 15 37ndash39]

The research groups from the mainland Taiwan andHong Kong of China have conducted a lot of investigationson ANAMMOX process including density and settleabilitymechanism of sludge modeling of packing pattern controlmechanism for floating sludge sequential biocatalyst addi-tion for inhibition recovery process recovery mechanismsillustration and so on to enhance the ANAMMOX processperformance and stability of the process After nearly 20

years of hard work the full-scale application of the ANAM-MOX has been successfully implemented for treatment ofmonosodium glutamate wastewater pharmaceutical wastew-ater and landfill leachate [40ndash44] A series of progress in bac-teria and process development were also forwarded whichcontributed significantly to help us understand the processand finally instigated researchers to operate and control thenovel autotrophic process The objective of this review isto present a detailed comparative summary of previous andcurrent researches on the progress in ANAMMOX bacteriadiscovery process development and the full-scale applicationin China

2 Recent Progress of ANAMMOX Bacteriain China

The ANAMMOX process is carried out by a group ofANAMMOX bacteria which are monophyletic group ofbacteria under Planctomycetes phylum Brocadiales orderand Candidatus taxonomic component [12] Till now at least5 genera and 13 species have been identified using culture-independentmolecular techniques [12] includingCandidatusldquoBrocadiardquo (Ca ldquoBrocadia anammoxidansrdquo Ca ldquoBrocadiafulgidardquo and Ca ldquoBrocadia sinicardquo) Candidatus ldquoKuene-nia stuttgartiensisrdquo Candidatus ldquoScalinduardquo (Ca ldquoScalinduabrodaerdquo Ca ldquoScalindua wagnerirdquo Ca ldquoScalindua sorokiniirdquoCa ldquoScalindua arabicardquo Ca ldquoScalindua sinooilfieldrdquo and CaldquoScalindua zhengheirdquo) Candidatus ldquoAnammoxoglobusrdquo (CaldquoAnammoxoglobus propionicusrdquo and Ca ldquoAnammoxoglobussulfaterdquo) Candidatus ldquoJettenia asiaticardquo

Candidatus Brocadia Kuenenia Scalindua Anammox-oglobus Jettenia genera have been isolated from differentwastewater treatment systems [6 17 19 45ndash47] only onegenus (Candidatus Scalindua) seems to be predominant inmarine ecosystems ranging from arctic to tropical regions[48ndash50] K stuttgartiensis is fresh water ANAMMOX bac-terium but could adapt to high salinity (up to 3) [51]Addition of organic acids like propionate or acetate favoredto proliferate the Brocadia fulgida or Anammoxoglobuspropionicus species with low fluxes of organicmatter [17 46]

Three new species of ANAMMOX bacteria (Candida-tus Brocadia sinica Candidatus Anammoxoglobus sulfateand Bacillus benzoevorans) have been discovered in ChinaAmong these three species Candidatus Brocadia sinica wasisolated from ANAMMOX reactors and other two species(Anammoxoglobus sulfate and Bacillus benzoevorans) wereidentified in sulfate removal reactors

21 Candidatus Brocadia sinica Hu et al [13] operated 8bioreactors with highly compact granulated sludge in dif-ferent physicochemical conditions Although the reactorswere operated in distinct variations in temperature (9ndash27∘C) or influent wastewater (inorganic medium glucoseor glutamate addition) these variations did not influencethe inhibition of ANAMMOX bacteria in reactor Vice-versathese changing conditions play an important role to grow uplarge population of the species which only can adapt to thischanging situation Especially a new ANAMMOX bacterial

BioMed Research International 3

(a) (b) (c) (d) (e)

Figure 1 Morphology of sulfate-dependent sludge (a) SEM ((b)ndash(e)) TEM ((a) sludge microbes (b) Cocci (c) Bacilli (d) morphologicalcharacteristics of Bacillus benzoevorans (times30000) and (e) structural characteristics of Bacillus benzoevorans (times70000)) [15 37]

species was enriched in five reactors among operated eightreactors which was then provisionally identified as ldquoCandi-datusBrocadia sinicardquo according to the taxonomic guidelinesThis indicated that ANAMMOX bacteria were found to beadapted to varying seeding influent conditions [51 52]

22 Sulfate-Dependent ANAMMOX Bacteria The researchgroups in China have discovered two novel species which areinevitable for sulfate removal and conducive for simultaneousammonium and sulfate removal process Liu et al [14]discovered a new species called ldquoAnammoxoglobus sulfaterdquowhich was the functional community in reactor to removeammonium and sulfate concomitantly Anammoxoglobussulfate mainly complete the conversion of ammonium andsulfate producing nitrite as intermediate product and thenthe nitrite diffused from cell to reactor solution across thebiological membrane At the same time other functionalPlanctomycetes bacteria performed the traditional ANAM-MOX process because both nitrite and ammonium wereavailable in the reactor due to diffusion Another reportshowed that Cai et al [15] conducted the isolation iden-tification and characterization of an autotrophic bacterialstrain for simultaneous anaerobic ammonium and sulfateremoval and identified a new species The newly discoveredspecies of ANAMMOX bacteria was identified as ldquoBacillusbenzoevoransrdquo which was able to use sulfate for anaerobicammonia oxidation The identified species will be conduciveto the understanding of microbial metabolism of sulfate-dependent ANAMMOX and will enrich microbial resources

The sulfate-dependent ANAMMOX bacteria are rod-shaped with flagellum and spore having a size of (07ndash10) times(24ndash35) 120583m The colony on the plate appeared light yellowround with a diameter about 1mm whose surface was wetand smooth Scan electron microscopy (SEM) displayed thatthe sulfate-dependent sludge was dominated by chains ofBacilli and Cocci The diameter of Cocci was around 09120583mand Bacilli diameter was around 08 120583m but length variedfrom 1 to 12120583m Bacterial cells were with inclusions (Figures1(a)ndash1(c)) [37] Another report agreed that sulfate removalBacillus benzoevorans was rod-shaped spore forming withflagellum which was discovered (Figures 1(d)ndash1(e)) byCai et al [15]

23 Natural Distribution of ANAMMOX Bacteria in ChinaANAMMOX bacteria have been detected in various natural

habitats such as anoxicmarine sediments and water columnsfreshwater sediments and water columns terrestrial ecosys-tems some special ecosystems (eg petroleum reservoirsleachate pharmaceutical waste and mangrove) and wastew-ater treatment systems ANAMMOX bacteria enumeratedisolated and identified from different ecosystems in differentareas of China have been illustrated in Table 1

The aforementioned data (Table 1) showed that ANAM-MOX bacteria were frequently identified from differentecosystems of different regional areas including terrestrial(soil wetland) ecosystem aquatic ecosystem (lake estuaryriver sea etc) and some specialized ecosystem (oil reser-voir MSG wastewater and pharmaceutical waste landfillleachate etc) In most cases Scalindua and Brocadia werefrequently isolated and identified while another genus ofANAMMOX bacteria was identified randomly So it is clearthat ANAMMOX bacteria were widely distributed in Chinaand among them Brocadia was predominant in fresh waterand Scalindua in sea water

3 Development of ANAMMOX Processin China

Most of the researchers used synthetic waste waters as influ-ent and other researchers used natural waste (monosodiumglutamate waste water sea lake river water etc) as influ-ent Synthetic wastewater was mostly prepared as influentwith the addition of ammonium and nitrite in the formof NH

4Cl(NH

4)2SO4and NaNO

2 A variety of reactor

types including sequencing batch reactor (SBR) [77] upflowanaerobic sludge blanket (UASB) [78] continuous stirredtank reactor (CSTR) [79] and membrane bioreactor (MBR)[80] have been tested for ANAMMOX startup and all showadvantages and disadvantages Usually 20 days maturedsludges are better for the reactor start up The carmine coloror bright red color settled sludge was more active than thefloating sludge

Reactors startup occurred by depositing the seedingsludge in reactor and subsequent addition of natural orsynthetic waste waters in reactors During the reactor startupinfluent concentrations below 100mgL of nitrite long HRT(few days to few hours) and completely anaerobic and darkconditions are conducive for quick and effective reactorstartup During reactor startup most of the researchersmaintained NH

4ndashN NO

2ndashN at 1 11 to 1 132 and outflow


Table 1 Natural distribution abundance and identification of ANAMMOX bacteria from different ecosystems in China

Ecosystem Abundance ANAMMOX Bacteria Area ReferenceSouth China Sea Tai Lam ChungWater Reservoir and Mai PoNature Reserve

NA Scalindua Jettenia KueneniaAnammoxoglobus and Brocadia South China [53]

South China Sea 119 times 104 to 717 times 104 Scalindua South China [54]

Jiaozhou Bay 389 times 101 to 389 times 106 Scalindua Jettenia Brocadia

Anammoxoglobus and Kuenenia East China [55]

Shengli Oilfield at Yellow RiverDelta 44 times 10

6 copiesg of soil Brocadia Kuenenia ScalinduaJettenia and Anammoxoglobus East China [56]

Paddy field NA Kuenenia AnammoxoglobusJettenia and Brocadia North China [57]

Freshwater sediments of theXinyi River NA Scalindua East China [58]

Different natural ecosystems NA Brocadia Kuenenia Scalindua andJettenia East China [12]

Pharmaceutical wastewater NA Photobacterium phosphoreum East China [40]Monosodium glutamate (MSG)wastewater NA Kuenenia East China [59]

Qiantang River NA Brocadia Kuenenia and Scalindua East China [13]

Honghe State Farm soil NA Scalindua NortheastChina [60]

Wetland 105 copiesg Scalindua Kuenenia Brocadia andJettenia South China [61]

Qiantang River NA AOA and AOB East China [62]

Paddy soil NA Anammoxoglobus Jettenia andAnammoxoglobus propionicus East China [63]


Paddy Soil Column NA Nitrososphaera Nitrosotalea andNitrosopumilus East China [65]

Jiaojiang Estuary NA Brocadia Kuenenia Scalindua andJettenia East China [66]

Agricultural soils 638 plusmn 042 times 104 to 369 plusmn 025 times 106 Brocadia Kuenenia Jettenia and

Anammoxoglobus East China [67]

Mai Po Nature Reserve NA Scalindua Kuenenia Scalindua andAnammoxoglobus South China [68]

Paddy soil 65 times 103 to 75 times 104 Brocadia and Jettenia North China [69]

Waste Lake NA Brocadia Kuinenia and Scalindua East China [70]NA not available AOA ammonia-oxidizing archaea AOB ammonia-oxidizing bacteria

concentration below 30mgLThe temperaturewas set at 35plusmn1∘C according to Tsushima et al [8] and the influent pH wascontrolled within the range of 68ndash70 [81]

31 High-Rate Nitrogen Removal Performance ANAMMOXresearch is promising and booming in China Manyresearchers focused on high performance of ANAMMOXactivity some researchers emphasized high loading rateand some other researchers plunged to discover somethingnew and promising for ANAMMOX development As aresult different kinds of ANAMMOX activity in lab scaleto full scale have been carried out and a lot of findings havebeen achieved in China The significant findings and crucialdevelopment in ANMMOX research have been highlightedin Table 2

Tabular data showed that many research groups obtainedNRRmore than 10 kg-Nm3d which was significantly higherthan the reported values all over the world Chen et al[29] obtained 57 kg-Nm3d nitrogen removal rate whichwas significantly a higher value compared to most of thereported values Tang et al [28] obtained a super high rateperformance with nitrogen removal rate (NRR) of 743ndash767 kg-Nm3d at 016ndash011 h HRT which was 3 times higherthan the previously reported highest value by Tsushimaet al [8] This was not only top value in China but also in thewhole world for laboratory scale reactor performance Tanget al [28] also obtained maximum sludge concentration inreactor (420ndash577 g-VSSL) which was 2-3 times higher thanpreviously reported values (007 g-VSSg-NH

4

+ndashN Trigoet al [22] 0088 g-VSSg-NH

4

+ndashN Strous et al [2] and 011 g-VSSg-NH

4

+ndashN van Dongen et al [82]) and the biomass


Table 2 Overview of high ANAMMOX performance in China

Reactor HRT Influent conc mgL Removal efficiency () NLR kg-Nm3d NRR kg-Nm3d ReferenceNH4ndashN NO2ndashN NH4ndashN NO2ndashN

UASB reactor 02 h 300 360 90 NA 891 743ndash767 [28]EGSB reactor 6ndash03 h 494 522 9468 9984 7784 5714 [29]EGSB reactor 15 h 6619 7672 717 941 2287 1865 [30]AGSB reactor 11 h 400 500 NA NA NA 1540 [26]UASB reactor NA 320ndash340 350ndash380 961 952 72 62 [27]Upflow filter system 199 h 305 304 742 924 734 611 [71]UASB reactor 012 h 1687 plusmn 209 2057 plusmn 231 9281 9435 NA 572 [72]ALR reactor 54 h 546 NA 944 NA 237 229 [73]UASB reactor 028 h 1687 plusmn 209 2057 plusmn 231 7845 9231 NA 228 [72]UBF reactor 154 h 9760 1280 8884 981 345 NA [74]SBR reactor 018 d 500 580 97 97 0156 NA [75]SBR reactor 3 d 268 345 836 100 NA NA [76]SBR reactor 15 h NA NA 809 88 NA NA [77]NA not available

doubling times were also shorter than the value reported in11 days by Strous et al [2] The research reports clarified thatthe highest performance was directly related to high settlingvelocity of sludge high specific ANAMMOX activity (SAA)and high ECP and Heme 119888 contents So it could be assumedthat high reactor performance would be obtained with thefollowing strategies

(i) The biomass concentrations in the reactorsmore than37 g-VSSL lead to compact packing of sludge whichdirectly favored the high reactor performance

(ii) The well-settled granules accumulation in reactorcontributes to the super high volumetric nitrogenremoval rates even at extremely high NLRs and shortHRTs

(iii) The high value of specific ANAMMOX activity (upto 56 kg-Nkg-VSSd) and short doubling time ofbacteria (below 11 days) could be regarded as the keyfactors to obtain the super high rate performance

(iv) Relatively high ECP and Heme 119888 content and lowPNPS ratios contributed to the ANAMMOX granu-lation which leads to high performance

32 Sulfate-Dependent ANAMMOX Process Simultaneousremoval of sulfate and ammonium by ANAMMOX processis a new biotechnology in wastewater treatment in whichammonium is oxidized with sulfate as electron acceptorunder anoxic conditionsThe new anaerobic ammonium andsulfate removal process can offer a great future potential foran energy-saving and environment-friendly alternative forsimultaneous nitrogen and sulfate removal from wastewaterIn 2001 the simultaneous ammonium and sulfate removalprocess was firstly discovered in an anaerobic fluidized-bedreactor by Fdz-Polanco et al [34] According to the report80 sulfate was converted to elemental sulfur accompaniedby ammonium oxidation to dinitrogen gas

321 Possible Reaction Mechanisms for Sulfate-DependentANAMMOX Anaerobic ammonium oxidation with sulfateis a microbiological sulfate reducing reaction The sulfate-dependent isolate used carbonate as carbon source ammo-nium as energy and nitrogen source and sulfate as electronacceptor Both SO

4

2minus andNH4

+ were chemically stable underanaerobic conditions but the reaction could be possible in thepresence of biological catalyst (sludge) The spontaneity of achemical reaction is associated with its free energy change(Δ119866) [83] Free energy for NH

4

+ is minus7937KJmol and forSO4

2minus is minus74463KJmol respectively Δ119866120579 of the sulfate andammonium reaction (2NH

4

+ + SO4

2minusrarr N2+ S + 4H

2O

(Δ119866120579 = minus4535KJmol)) is minus4535 KJmol So it indicatedthat the simultaneous reaction could occur Practically thespontaneity of chemical processes is conducted by Δ119866 ifthe absolute value of its Δ119866120579 is less than 46KJmol [20]Thus Δ119866 at different substrate concentrations is calculatedaccording to the equation Δ119866 = Δ119866120579 + 119877119879 ln119876 (119876 isreaction quotient) If the Δ119866 value under tested conditionschanged from positive to negative by increasing the substrateconcentrations the reactions between NH

4

+ndashN and SO4

2minus

were therefore enhanced based on this principle On theother hand optimal nutrient and environmental conditionsΔ119866 also play an important role in the process realizationSulfate reducing ANAMMOX bacteria (SRB) are a kindof obligate anaerobic bacteria and only viable when theoxidation reduction potential (ORP) is belowminus100mVwhichwas fulfilled by flushing the reactor with N

2[84] This higher

substrate concentration and lower (below minus100mV) oxida-tion reduction potential (ORP) phenomenon contributed tothe simultaneous sulfate and ammonium removal

Fdz-Polanco et al [34] explanation showed that auto-trophic anaerobic ammonium oxidation and sulfate deoxida-tion occurred by three consecutive biochemical reactions (1)(2) and (3)


(i) Ammonium was partly oxidized by sulfate and viceversa sulfate was deoxidized to produce nitrite andsulfide

(ii) Then part of the produced nitrite was reduced bysulfide and was converted to dinitrogen gas andelemental sulfur

(iii) Finally nitrite-dependant anaerobic ammonium oxi-dation (ANAMMOX) took place

(iv) Being in a reduced form sulfide can be oxidized intoeither elemental sulfur or sulfate depending on theinitial ratio between sulfide and nitrite [85]Themainproducts are likely to be elemental sulfur and sulfateat a ratio of 3 4 (4) Sulfide and nitrite molecularratio must be critically controlled to prevent sulfateproduction

3SO4

2minus+ 4NH

4

+997888rarr 3S

2

minus+ 4NO

2

minus+ 4H2O + 8H+

(ammonium oxidation process)(1)

3S2

minus+ 2NO

2

minus+ 8H+ 997888rarr N

2+ 3S + 4H

2O

(nitrite reduction process)(2)

2NO2

minus+ 2NH

4

+997888rarr 2N

2+ 4H2O

(ANAMMOX process)(3)

3S2

minus+ 4NO

2

minus+ 4H2O 997888rarr SO

4

2minus+ 2S + 8OHminus + 2N

2

(4)

NH4

++

1

2

SO4

2minus997888rarr

1

2

N2+

1

2

S + 2H2O (5)

The experimental data revealed that high substrate con-centrations and low oxidation-reduction potential (ORP)enhanced the biological reaction From the above reactionswe can conclude that ammonium reactedwith sulfate andwasoxidized to nitrite (intermediate product) inside sludge gran-ule (bacterial cell) by oxidation process and concomitantlysulfate is deoxidizedThen the produced nitrite diffused fromsludge (bacterial cell) to reactor and reacted with ammo-nium in the reactor by ANAMMOX process and eventuallyproduced nitrogen gas In the terminal stage ammoniumand sulfate reacted with each other and were converted tonitrogen gas and solid sulfur

322 Sulfate-Dependent ANAMMOX Researches in ChinaMost of the research groups had used (NH

4)2SO4and

NaNO2substrates as influent in reactor for N and S source

respectively [15 37 38] Vice versa some researchers usedonly (NH

4)2SO4as sole substrate in influent for N and S

source [14]Sulfate-dependent ANAMMOX bacterial growth is too

slow or the doubling time is too long and thus it takes moretime to start up the reactor The anaerobic digested sludgewas cultivated in an anaerobic reactor for three years andthen the sludge became capable to oxidize ammonium withsulfate anaerobically The sludge volume increase of sulfate

reducing ANAMMOX was trivial because a little bit biomassdevelopment was achieved after a long-term reactor opera-tion Reaction between sulfate and ammonium that occurredrarely was difficult to observe but it became possible onlywith the coexisting of sulfate reducing and ANAMMOX bac-teria Although some research groups revealed the reactionmechanisms for simultaneous removal of ammonium andsulfate only very few researches on this topic were carried outdue to requirement of long-term operation and minusculesuccess probability It is found that some research groupsconducted research on this and disclosed promising ideaand application The reports of recent researches have beenpresented in Table 3

Cai et al [15] investigated simultaneous ammonium andsulfur removal ANAMMOX process and phylogeneticallyanalyzed a sulfate reducing strain which was related toBacillus benzoevorans The investigation also revealed thatthe maximum 444 and 40 ammonia and sulfate removalrates even at pH 85 and stoichiometric ratio 201 1 developedby Fdz-Polanco et al [34] were obtained respectively Yanget al [38] also reported 40 and 30 removal efficiencies ofammoniumand sulfate atmolar ratio of ammonium to sulfateconsumption of 2 1 respectively in an anaerobic bioreactorfilled with granular activated carbon Another report of Liuet al [14] disclosed that a new species of Brocadia genusnamely ldquoAnammoxoglobus sulfaterdquo which was discoveredfrom a ammonium and sulfate enriched niche and revealedthat this species played a critical role in the ammonium oxi-dization and sulfate reductionThe species mainly completedthe conversion of ammonium and sulfate and then producedan intermediate product nitrite which diffused from bacteria(sludge) to reactor solution across the biological membraneThen some other functional Planctomycetes bacteria performthe traditional ANAMMOX process due to presence ofammonium and nitrite So the investigation indicated thatthe full conversion of ammonium and sulfate occurred withthe coexistence of ANAMMOXand sulfate reducing bacteriaIn this investigation nonwoven rotating biological contactorreactor was preferred over some other types of reactorsbecause it combines the advantages of a biofilm reactor(large specific surface area) and adsorption characteristicswith the improvement of the gas-liquid transfer rate (goodmixture of substrates and flux) Zhang et al [37] cultivatedthe anaerobic digested sludge in an anaerobic reactor forthree years and found that after long-term operation thesludge became capable to oxidize ammonium with sulfateanaerobically The obtained results significantly contributedto the sulfate-dependent ANAMMOX research in the world

Sulfate reducingANAMMOXprocess was sensitive to pHand temperature and it is reported that reactor performancewas inhibited at pHand temperature higher than 85 and 30∘C[15] respectively Liu et al [14] reported that simultaneousremoval process might be hindered if there is no coexistenceof sulfate reducing bacteria and autotrophic ANAMMOXbacteria According to Yang et al [38] ammonium andsulfate removal efficiencies might be affected by somemiddlemedium such as nitrite H

2S and sulfur Supporting to

this report Fdz-Polanco et al [34] reported a completeloss of ANAMMOX activity when the nitrite concentration


Table3Overviewof

thes

ulfate-dependent

ANAMMOXprocessinvestig

ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


remained above 5mM (70 g NO2

minusndashNm3) for a long period(12 h) Another report surmised that sulfide might toxic tomicroorganisms [86]

323 Future Prospect of Sulfate-Dependent ANAMMOX Pro-cess in China It can be proposed that sulfate-dependentANAMMOX researches have an inspiring future and devel-opment and application in China with the followingprospects

(i) Comparing to ANAMMOX bacteria the biomassproduction or doubling time of sulfate-dependentANAMMOX is too slow This limitation could beovercome by enrichment of reactor with special care

(ii) Newly discovered two species Bacillus benzoevoransand Brocadia ldquoAnammoxoglobus sulfaterdquo could beused ubiquitous for simultaneous removal of sulfateand ammonium

(iii) Pure chemical reaction between ammonium andsulfate without microorganisms was not possible Somassive biomass production could open a new wayfor vigorous application

(iv) Sulfate-dependent ANAMMOX performed good incoexistence condition of biomass which could playan important role in extensive reactor performanceimprovement

33 ANAMMOX Process with Sequential Biocatalysts Addi-tion Tang et al [40] observed that the pharmaceuticalwastewater possessed severe acute toxicity with a relativeluminosity value of 346 plusmn 045 and the conventionalANAMMOX process was not suitable for nitrogen removalfrom this wastewater due to cumulative toxicity Finally thetoxicity of the pharmaceutical wastewater was successfullyavoided with the introduction of a novel SBA-ANAMMOXprocess (ANAMMOX process with sequential biocatalystaddition) and the nitrogen removal rate was also significantlyenhanced to 94 kg-Nm3d (by adding 0025 g VSSd freshseeding sludge in reactor) [40] So the application of SBA-ANAMMOX process in refractory ammonium-rich wastew-ater is encouraging

There may be a question of how the sequential additionof fresh sludge improves the reactor performance Exogenousaddition of high-activity ANAMMOX biomass into the reac-tor system can supplement the required bacterial amount andalso can increase the density of sludge in reactor which even-tually enhanced the nitrogen removal performance Delib-erate addition of high-activity ANAMMOX seeding sludgeinto reactor led to the addition of some unknown growthfactors contained in the granules which showed strongerresistance to toxic substances and eventually enhanced thegrowth of ANAMMOX bacteria [40] The granules additionsubsequently contributed to the high-rate nitrogen removalperformance at the low biocatalyst addition rate So theanswer is that addition of fresh sludge in the reactor increasedthe settleability density and growth conditions of the existingsludge which help to rejuvenate the existing sludge activityand thus improve the reactor performance

Li et al [27] disclosed that the returning of washoutsludge to the reactor played an important role in promptrecovery of ANAMMOX performance Yang et al [87]proposed that addition of fresh ANAMMOX sludge toreactor may improve the living conditions of ANAMMOXbacteria and by adding 201 gL (VSS) sludge (on day 135)and 210 gL (VSS) sludge (on day 170) in the inhibitedreactor they obtained increasing nitrogen removal rate from0025 to 0069 kg-Nm3d (on day 135) and from 0069 to0323 kg-Nm3d (on day 170) respectively By operatingthe conventional ANAMMOX reactor and SBA-ANAMMOXreactor in parallel Tang et al [40] found that the ammo-nium and nitrite removal efficiencies for SBA-ANAMMOXreactor were 804ndash862 and 926ndash948 respectively whilethe removal efficiencies for conventional reactor were only19ndash138 and 145ndash342 respectively This indicated thatSBA-ANAMMOX process could successfully overcome thetoxic effects of refractory ammonium-rich pharmaceuticalwastewater From different research reports it could beconcluded that sequential sludge addition is an effective andsustainable way to improve the reactor performance Thusthe cost-effective and high-rate SBA-ANAMMOX process isa promising biotechnology with enormous advantages thatcould treat ammonium-rich wastewaters effectively

4 Morphological Study ofANAMMOX Granules

41 General Characteristics of ANAMMOX Granules

Color The color of high performing fresh seeding ANAM-MOX sludge tended to be bright red or carmine (Figure 2)Sludge color is an indicator of sludge viability and perfor-mance If the sludge color changed from carmine to pale redor black it indicated that the sludge activity reduced

After a long-term reactor operation the sludge becamepale red due to a decrease of Heme 119888 and became blackbecause the sludge did not get a substrate for a long time

Size The average diameter of ANAMMOX sludge granulevaried from 22 to 25mm with VSSTSS at 87 and amongthem the larger than 2mm granules were predominant(68ndash71) [28] Sludge size is also an indicator of reactorperformance Large sludge has low settleability and smallsludge has high settleability High settleability is a goodindicator for effective reactor performance The diameter ofthe floating granules was 231ndash696mm with an average of458 plusmn 122mm while that of the settling granules was 086ndash698mm with an average of 296 plusmn 099mm [89] Largesludge has more gas pockets and gas volume than smallsludge [89] It implied that the ANAMMOX granules with adiameter larger than 4mm had a strong trend to float in highrate reactors due to accumulation of dinitrogen gas in gaspockets [28] At high removal rate more gas produced insidethe sludge which lead to decrease the settleability of sludgeand thus larger sludge became floating and smaller sludge


(a) (b)

Figure 2 The granules in high-rate ANAMMOX UASB reactor (a) and the image of ANAMMOX granules (b) [88]

remained settled [89] Floating behaviors of sludge decreasethe reactor performance

Density Sludge density is another indicator of high activityreactor performance The density of ANAMMOX granulesin reactors was measured by Tang et al [28] and it wasabout 103 gmL the specific density of the ANAMMOXgranules (91 to 120 g-VSSL-granules) was also comparableto aerobic granules (40 to 70 g-VSSL-granules) and high-loaded denitrifying granules (128 to 136 g-VSSL-granulesFranco et al [90]) Sludge density is proportional to reactorperformance and alternatively sludge size is disproportionalto sludge density

Settling Velocity of ANAMMOX Granules According to thewell-known Stokes equation the settling velocity of ANAM-MOX granules is closely related to their size and densityThe increasing size and density might result in a significantincrease of settling velocity of granules [91] The floatingANAMMOX granules did not settle so only the settlingvelocity of settling ANAMMOX granules was determinedThe settling velocity increased with the increase of sludgediameter and high settling velocity (73 to 88mh) wasobtained by Lu et al [92]

Relationship of Settleability with Structure and Density Thediameter and the density were two key factors for thesettleability of ANAMMOX granules in the reactors Thesettling velocity of ANAMMOX granules increased withthe increasing diameter while the density of ANAMMOXgranules decreased with the increasing diameter MatureANAMMOX granules settled very well at velocities of 41to 79mh which were similar to the settling velocities ofthe methanogenic granules (eg 529mh) and at least twotimes greater than those of the flocculated ANAMMOXsludge [41] The significant increase in settling velocities

indicated that the ANAMMOX granules had a highly denseand compact structure which is more effective for sludge-effluent separation in the treatment system

42 Morphology of ANAMMOX Granules The structure ofthe microbial granules developed in reactors was observedby means of SEM and TEM The scanning electron micro-graphs (SEM) showed typical coccoid-shaped cells as thedominant microorganisms on the granule surface embeddedin an extracellular polysaccharide (EPS) matrix (Figure 3(a))very similar to those reported by others [53 93 94]Figure 3(b) showed the typical crescent-shaped ANAMMOXcells obtained via transmission electronmicrograph of chem-ically fixed ANAMMOX cells [95] The scanning electronmicrographs represented by Tang et al [28] showed that ared-colored mature ANAMMOX granule was characterizedby a cauliflower-like shape The granular surface mainlyconsisted of spherical and elliptical bacteria few or evenno bacilli and filamentous bacteria were observed in thetwo reactor enrichments suggesting that the ANAMMOXbacteria dominated after enrichment [28]

43 Chemical Properties of ANAMMOX Granules

431 Extracellular Polymers Before discovery of granula-tion mechanism researchers used single ANAMMOX bac-terial cells for reactor operation After discovery of sludgegranulation process plenty of researchers operated reactorswith sludge and pointed out that sludge mediated reactorperformances were obviously higher than bacterial medi-ated reactor performance So it was of a great demandto the researchers to explore the possibility of granulationof ANAMMOX biomass and its application for high per-formance The EPS containing bacteria played vital rolein the formation of granules in bioreactors [96ndash99] ECPs


Appearance of granule Part of appearance Part of section

(a)

Seeding sludge Day 140 Day 250

(b)

Figure 3 (a) SEM images of the ANAMMOX granular sludge (b) TEM images of the ANAMMOX bacteria in sludge in the granulationprocess [41]

could physically bridge neighboring cells by altering thenegative charges on bacterial surface [99] and thus gran-ulation may be facilitated by large secretion of ECP EPSsare distributed throughout the ANAMMOX bacterial surfacewhich attracted scientists to study it with a view of obtainingan efficient sustainable and stable sludge granulation forhigh rate reactor operation

The microbial ECPs are a rich matrix of polymers whichmainly constituted of polysaccharides and proteins [98]The EPS of each gram of ANAMMOX granule (in VSS)contained 832 plusmn 79mg carbohydrates and 427 plusmn 65mg pro-teins granules [41] The EPS content of autotrophic ANAM-MOX granules (125mg EPSg-VSS) is significantly higherthan EPS content (10ndash91mg EPSg-VSS) of heterotrophicmethanogenic granules [41] The proteincarbohydrate ratio(051) of autotrophic ANAMMOX granule is lower thanheterotrophic methanogenic granules (12ndash40) [41] Thisindicated that protein might be the key constituent formethanogenic granules and contrarily carbohydrate mightbe the major constituent for ANAMMOX granules Thisinformation postulated that carbohydrate might play moreimportant role than protein in the formation of ANAMMOXgranulesThe large amount of glycosylation proteins encodedby the ldquoCandidatus Kueneniardquo genome is supportive of thissuggestion [17] Tang et al [28] determined the ECP contentat different nitrogen removal levels and summarized thatboth polysaccharide and protein contents increased with

the increasing nitrogen removal rate (NRR) The investiga-tion also revealed that the polysaccharide contents (718 plusmn23mgg-VSS) increased slowly as compared to the pro-tein contents (1644 plusmn 93mgg-VSS) The CLSM analysis(Figure 4) showed mixed patterns of cells and EPS distri-butions in the ANAMMOX granules [41] The EPSs weredistributed throughout the granules while the bacteria weremainly situated in the outer layer of the granule

The proteins to polysaccharides ratio (PNPS) was gener-ally used to assess the granular settleability and strength [90100ndash104] Various researchers investigated EPS and pointedout that the higher PNPS ratio of microbial granules led tolower strength and weaker settleability [100ndash103] thus thesludge floating or foaming would occurr easily [90 104]The PNPS ratio of the ANAMMOX granules (051) wasalso low in contrast to other microbial granules (12ndash40)recommending a greater granular stability [90] Tang et al[28] determined the ECP contents of the floated granulesand found that extracellular proteins and PNPS ratios ofthe floated ANAMMOX granules (388ndash409) at high NRRsand HLRs were significantly higher than the counterpartsof well-settled (240ndash265) granules The overproduction ofextracellular proteins might be a potential cause resulting inthe severe sludge washout from the UASB reactors

432 Heme 119888 Content Sludge color is an indicator of highactivity ANAMMOX granule and the sludge color varied


ANAMMOX sludge

(a)

Section 1 Section 2 Section 3

(b)

Figure 4 (a) EPSs at outer surface of carmine red ANAMMOX sludge (b) CLSM images of the 50120583m cryosections of the ANAMMOXgranule from surface to center Cells were stained with SYTO9 (green) and polysaccharides were stained with concanavalin A (red) [28 41]

from carmine red to pale red brownish or black High-load ANAMMOX granules are uniquely carmine (Figure 4)in color It was well accepted that Heme 119888 played a vital roleto develop carmine color in sludge granule Sludge color wasdirectly related to reactor performance and thus researcherspenetrated their concentration to reveal the role of Heme 119888and its evaluation

ANAMMOX bacteria have some vital enzymes such ashydrazine synthase (HZS) hydroxylamine oxidoreductase(HAO) and hydrazine oxidase [105] which are rich inANAMMOX bacteria cell and involved in substance andenergy metabolism Recent researches report postulated thatHeme 119888 is the indispensible part of these key enzymes ofANAMMOX bacteria [106 107] and the content of Heme 119888might be involved in ANAMMOX activity and other relativeactivities [108] Heme 119888 also plays an important role for thedevelopment of carmine color of ANAMMOX sludge It isassumed that the content of heme 119888 might be changed withthe fluctuation of nitrogen removal rates (NRR) and Tanget al [28] disclosed that the content of Heme 119888 increasedsignificantly with the increasing NRR Tang et al [28]showed that the Heme 119888 content was 07ndash14mmolg-VSS atNRR lower than 10 kg-Nm3d and the content dramaticallyreached 97ndash108mmolg VSS at NRR higher than 70 kg-Nm3d Thus the increase of Heme 119888 content was associatedwith the increase of ANAMMOX bacterial numbers result-ing in high specific ANAMMOX activity (SAA) Finally itcould be concluded that the changes of Heme 119888 content couldrepresent the growth status of ANAMMOX consortia andHeme 119888 level could be used to evaluate the relative activityof ANAMMOX microorganisms and to imply the recoveryof ANAMMOX reactor performance Carmine red grey andblack color sludges are presented in Figure 4(a) The redcolored is due to high Heme 119888 content grey color due to lowcontent and back is due to absence of Heme 119888 that occurredby blockage of sludge

44 Structure of ANAMMOX Granules and Granulation ofANAMMOX Biomass

441 Structure of ANAMMOX Granules According to theobservation of Lu et al [92] under light microscope andelectron microscope the structure of ANAMMOX granules

included granule subunit microbial cell cluster and singlecell (Figure 5)

(i) Granule Anammox granules were irregular in shape witha diameter of 296 plusmn 099mm [92] and the surface of granulewas rough The granule was broken along the furrow and thebroken parts were known as subunits Subunits were linkedto each other by EPS and filamentous bacteria

(ii) Subunit SEM and TEM micrographs of differentresearches mentioned that filamentous bacteria were pre-dominant both in inner and outer surface of ANMMOXsubunits Subunit or ldquoEPS-filamentous bacteriardquo bands weresegmented into several compartments which were called cellclusters

(iii) Microbial Cell Cluster In cell clusters microbial cellswere aggregated close to each other by EPSs and filamentousbacteria and the cluster size varied from few to 200 120583mThe microbial cell clusters were composed of ANAMMOXbacteria-like cells

(iv) Interstitial Voids Subunits microbial cell clusters ormicrobial cells were separated from each other by interstitialspace which was known as interstitial voids Interstitial voidswere surrounded by EPSs and were filled with water or dini-trogen gas The sizes of interstitial voids were proportionalto granular size and voids could serve as water channel andgas tunnel In the beginning interstitial voids were filled withwater and worked as water channel to transport substrates(NH4

+ and NO2

minus) and products and they were 80 nm indiameter [109 110] With the activities of microbial cells thetransported substrates were converted to dinitrogen gas andthis gas accumulated inside the ANAMMOX granules andthe interstitial voidswere finally used as gas tunnels for releaseof dinitrogen gas

442 Granulation of ANAMMOX Biomass In the beginningof ANAMMOX process discovery the low influent loadingrate or moderate influent loading reactors were operatedwith single ANAMMOX bacteria and there were no problemin reactor operation But when high loading rate reactorsoperation started with an extremely high upflow velocity


[andashf] indicate the granulation[gndashj] indicate the mass transfer[kndashn] indicate the floatation

(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)

Figure 5 Structures of ANAMMOX granules DMP ((b) (m)-(n)) SEM ((a) (c) (e)ndash(h) (k) and (l)) and TEM ((d) (f) and (i)-(j)) (a)One ANAMMOX granule composed of subunits (marked with closed curve) and ditches (indicated with arrows) separating the subunits(b) An ANAMMOX granule (on the top left corner) broken into several subunits (c) Microbial cell clusters (marked with closed curve)connected by the filamentous bacteria and (d) separated by filamentous bacteria-EPS bands (indicated with rectangles) (e) Interstitial spacethe honeycomb-like structures (indicated with circles) (f) ANAMMOX bacteria-like cells (marked with a circle) (g) Ditches (indicated withyellow arrows) between subunits in the exterior of granules (h) Interstitial voids (indicatedwith yellow arrows) betweenmicrobial cell clustersin the exterior of granules and (i) in the interior of granules (indicated with rectangles) (j) Gas tunnels between microbial cells (indicatedwith arrows) (k) Small gas pocket (marked with rectangle) (l) Gas pocket of a settling granule formed by inflation of dinitrogen gas (m) Gaspocket of a floating granule (indicated with closed curve) (n) A broken floating ANAMMOX granule formed by the burst of dinitrogen gas[92]


GranulationFilamentous bacteria

ldquoimmeshing and bridgingrdquo effect

Aggregation

Small ANAMMOX cell cluster

ANAMMOX bacteria

Zoom outSmall granule

Composite

Large ANAMMOX cell cluster

GranuleGrow-up

Figure 6 The hypothesized mechanism for granulation and floatation of ANAMMOX biomass Underlined are the microbial structuresobserved in this study [92]

large influent loading rate and large gas production of theANAMMOX biomass were washed out with effluent dueto poor settleability [111] So granulation of ANAMMOXbiomass was inevitable to overcome the biomass washout andto enhance reactor performance Thus researchers empha-sized this and their microscopic observations assumed thatgranulation process accomplished with the sequential aggre-gation of microbial cells cell clusters and subunit

ANAMMOX sludge granulation started from ANAM-MOX bacterial cell With an extremely slow growth rate theANAMMOX bacteria have an affinity to accumulate EPSs[28] and this leads to granulation [22 112] ANAMMOXgran-ule has been investigated thoroughly in various bioreactors[22 82 113ndash116] but there is very few studies and findingsabout the granulation mechanism According to microscopicobservation of Lu et al [92] the granulation of ANAMMOXbiomass granulation (Figure 6) in high-rate reactors could beaccomplished in three consecutive steps

(i) Formation of Microbial Cell Cluster In a high influentloading reactor the bacteria collide with each other dueto high flow rate and high shear force At the time ofcollision the bacteria are entrapped with each other by theirimmobilized sticky EPSs and form an aggregate of bacterialcell called cell cluster

(ii) Formation of ANAMMOX Subunit Then the microbialcell clusters were assembled together with the help of fila-mentous bacteria to form an aggregate of cell cluster whichis called ANAMMOX subunits The filamentous bacteriadeparted from ANAMMOX subunits and then gas tunneldeveloped in the interstitial space among microbial cellclusters

(iii) Formation of ANAMMOX Granule The ANAMMOXsubunits in the reactors collided with each other due to thehigh inflow rate and high gas production and then assembled

together with immobilized EPSs and finally produced ANM-MOX granules (Figure 6)

45 Floatation and Control of ANAMMOX Granule

451 Floatation of ANAMMOX Biomass All of the ANAM-MOX granules have gas tunnels and gas pockets In highloading reactors with high activity of ANAMMOX bacteriathe gas bubbles are produced in gas tunnels and gas pocketsThe gas bubbles entrapped in gas pockets were supposed tobe the key factor to cause sludge floatation After the hollowswere filled with gas bubbles the ANAMMOX granules wouldfloat and be washed out of reactor leading to failure ofANAMMOX process The granule floatation was found to bean important factor that causes instability or even collapseof ANAMMOX reactor Facing these problems some Chineseresearch groups [92 113] conducted research and revealed theeffective strategy to overcome the floatation and to restorereactor performance

Inside the floating granules the gas tunnels were closedand inside settled sludge the tunnels were opened This phe-nomenon suggested that the gas inside settled sludge couldbe released easily but the gas inside floating sludge could notbe released due to clogging of the gas tunnels As a result thesludges were floated at high dinitrogen releasing stage andthese floatings declined the reactor performances So therewas a necessity to find out the reason of sludge floatationand controlmechanism of floatation for restoration of reactorperformance The floatation of ANAMMOX biofilm wasextensively investigated and mechanism of sludge floatation(Figure 7) could be explained in three sequential phases [92]such as (i) formation of gas tunnel (ii) formation of gaspocket and (iii) floatation of sludge granule

(i) Formation of Gas Tunnel It has been reported that theANAMMOX bacteria tend to grow together [22] and thus


Floatation

Large settlinggranule Floating granule Broken granule

Gas tunnel blockedby excessive EPs

Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)

Figure 7 (a)The hypothesizedmechanisms for floatation of ANAMMOX sludge (b) granules in different operation phases floating granules(A B) settling granules (C D) and mechanically broken granules (E F) in reactor Both the floating and settling granules contained gaspockets marked Gf and Gs and gas tunnels marked Tf and Ts respectively [92 113]

the ANAMMOX granules were supposed to develop fromsmall sludge granules by adhering to each other and hollowspace inside granules was supposed to develop from thegaps between small sludge granules The substrates were(ammonia and nitrite) diffused into the bacterial cells fromreactor and subsequently dinitrogen gas was produced insidethe sludge due to bacteria activities and accumulated as gasbubblesThen the gas bubbles tend to be released from sludgethrough the interstitial gaps between small sludge gran-ules and thus create gas tunnels Microscopic observationreported that a lot of gas tunnels developed for releasing gasoutside of the sludge through these tunnels The gas tunnelsinside settled sludge were open but inside floating sludgewere closed

(ii) Formation of Gas PocketWith increasing influent rate andhigh reactor performance extensive dinitrogen gas was pro-ducedThe produced dinitrogen gas entrapped with ANAM-MOX granules for maintaining a balance of production andrelease [114] The excessive dinitrogen gas inside the granulesmoved to and fro which created a larger resistance and higherpressure These larger resistance and higher pressure wereforced to enlarge the loose of interstitial voids between cellclusters of subunit and thus led to develop gas pocket Thegas pockets inside the granules were connected to outsideenvironment through gas tunnels

(iii) Floatation of ANAMMOX Granules According toresearch reports EPSs production increased with the increas-ing loading rates [28] and thus extensive EPSs were producedat high loading rates which led to clog the gas tunnels Highloading rate favored the ANAMMOX sludge to produce hugeamount of dinitrogen gas which could not be released outsideof sludge through the tunnels due to clogging of gas tunnels[113] As a result the excessive gas bubbles were entrappedinside gas tunnels The entrapped dinitrogen gas surpasseda critical value (57 VV) and thus the density of granules

would be lower than that of water which led to the floatationof ANAMMOX granules

452 Control Strategy for Granule Floatation Chen et al[113] assumed that the floating granules have blocked gastunnels and gas pockets and thus the dinitrogen gas could notbe released from sludge which caused floating of the sludgesThen the floating sludges were washed out with effluent fromreactor which caused deterioration of reactor performanceand thus lead to failure of ANAMMOXprocessThis washoutobstacle compelled the researchers to find out the possibleway to overcome this obstacle

The floating granules were taken out of the reactor andbroken into small pieces and returned into reactor to over-come the frequent floating problem of ANAMMOX sludgeAfter the reactor was operated with the control strategy thefloatation and washout of ANAMMOX sludge became con-strained and the performance improvedThe broken granules(BGs) had various size with diameters mainly of 05ndash26mmand thewet density of broken granules was higher than that ofsettled granules reaching 10477 plusmn 51mgL [113] The controlstrategy improved the performance of ANAMMOX reactorSo ldquocollecting-breaking-returningrdquo procedure (Figure 7) wassuggested to be an effective control strategy to solve granulefloatation and improve reactor performance Alternativelythe collecting-breaking-returning procedure in some casesmight disturb the microbial ecology (death of bacteriareduction of ANAMMOX activity loss of biomass particlesetc) inside granules and impair the ANAMMOX activityFurthermore the recovery of the reactor performance mightbe a bit long since the reformation of ANAMMOX granuleswas needed

46 Packing Pattern and Packing Density of ANAMMOXSludge The pore volume and sludge concentration insideANAMMOX reactors are related to the packing patterns of


(a) (b)

Figure 8 Images of the pilot-scale ANAMMOX reactor (a) and packing materials (b) [117]

ANAMMOX granules The packing patterns are character-ized with the coordination number and packing pattern var-ied depending on coordination numbers Previous researchreports explained that packing patterns were responsible forpore volume and sludge density and subsequently sludgedensity directly led to reactor performance According to thereports the sludge density 52ndash55 [88] showed themaximumreactor performance Different types of packing patternsrepresent different sludge density and variable reactor per-formance So there was a need to find out the appropriatepacking pattern for optimum reactor performance

Tang et al [88] initially developed the packing patternof granular sludge following the principles and theories ofcrystal lattice patterns [118] A series of relationships amongpacking density sludge concentration coordination numbernitrogen removal performance and HRT were evaluatedFinally the mathematic equation of the packing patternconcerning the nitrogen removal rate (119877) sludge concen-tration (119862

119883) and the substrate loading (119888) was constructed

as shown in (6) Depending on this packing pattern thenitrogen removal performance could be illustrated by thesludge concentration and substrate load

119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883

120588 granule sdot SV)

016

119862023

(6)

where 119902 is specific activity of the sludge 120588 granule is thedensity of granular sludge and SV is the sludge volume

The reactor performance could be evaluated with thedeveloped packing pattern Sludge density pore volume andsludge concentration in reactor could be investigatedwith thehelp of packing pattern Based on the sensitivity analysis thefollowing conclusions could be drawn When 119862

119883is equal to

378 gL the sludge concentration and substrate loading ratewere equally important in contributing to the high conversioncapacity of the ANAMMOX UASB reactor When 119862

119883was

less than 378 gL 119862119883was more sensitive than 119888 indicating

that it was more effective to enhance sludge concentrationfor improvement of conversion capacity while when 119862

119883

was higher than 378 gL 119888 was more sensitive which meantthat elevating substrate loading was an advisable strategy forANAMMOX reactor operation

5 Application of ANAMMOX Process in China

In China ANAMMOX research area is growing day by dayMost of the researches have been conducted in laboratoryscale Some ANAMMOX research groups also carried outANAMMOX research in pilot-scales and found significantoutcomes Different research groups are operating pilot-scale ANAMMOX process to treat different types of wasteand finally succeeded to protect the ecosystem with theirmaximum capability The pilot-scale operation is at the pointfrom where the researchers opted to devise for full scaleoperation Some pilot-scale ANAMMOX applications havebeen highlighted in Table 4 and Figure 8

The above-mentioned data (Table 4) showed that pilotscale reactors were operated with working volume thatranged between 0020 and 225m3 and different types ofwaste water were treated by applying this process Thisimplied that pilot-scale reactor operation in China is signif-icant in the transitional point from the development pointof view An et al [117] successfully operated a pilot-scaleANAMMOX reactor to treat dry-spun acrylic fiber wastew-ater (DAFW) which is depicted in Figure 8 By controllingthe reactor temperature and SS in influent the removalefficiencies of ammonium and nitrite were 85 and 90respectively

Nitrogen waste is one of the vital pollution problems inChinaWith the increase of Chinese economy theANMMOXresearches tend to move in full-scale treatment plant SoChina is the promising and largest market for ANAM-MOX waste treatments In the Netherlands the first full-scale granular ANAMMOX reactor was commenced at thewastewater treatment plant of Water board Holland se Deltain Rotterdam in 2006 [16 99] This full-scale ANMMOXtreatment plant was themilestone for commercial applicationof ANAMMOX process The first full-scale reactor volumewas 70m3 which was 7000-fold from 10 L lab-scale experi-ment So far more than 30 full-scale divergent plants are inoperation throughout the world mostly in Austria ChinaJapan the Netherlands and USA All of these plants wereestablished emphasizing ANAMMOX process and finally hasbecome a commercial technique In 2009 EnvironmentalTechnology (Shanghai) released the news that an agreementhad been reached to build the worldrsquos largest ANAMMOXbased wastewater treatment plant in China [44]


Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable


Table 5 Brief description of full scale ANAMMOX plants in China

CompanyInstitution Area Substrate Reactor volumem3

Designed loadkg-Nd Year Reference

Zhejiang University Zhejiang Pharmaceutical waste 10 5 2010 [40]

Zhejiang University Zhejiang Monosodium glutamatewastewater 60 5 2008 Personal

communicationNational Chiao TungUniversity Taiwan Landfill leachate 384 304m3dlowast 2006 [43]

Angel Yeast Yichang Yeast production 500 1000 2009

Paque [44]

Meihua I Tongliao Monosodium glutamate(MSG) 6600 11000 2009

Meihua II Tongliao MSG 4100 9000 2010Shandong Xiangrui Shandong Corn starch and MSG 4300 6090 2011Jiangsu HangguangBio-engineering Wuxi Sweetener 1600 2180 2011

Xinjiang Meihua AminoAcid Wujiaqu MSG 5400 10710 2011

Kuaijishan hoaxing Winery Shaoxing Distillery 560 900 2011lowastAverage leachate flow of 304m3d with a sludge retention time between 12 and 18 d

Figure 9 Full-scale 11000 kg-Nd one-step ANAMMOX installa-tion at the Tongliao Meihua Company in China Courtesy Paques[121]

At the Tongliao Meihua industrial complex one stepANAMMOX reactor with design capacity of 11000 kg-Ndhas been implemented byPaquewhich could treat the effluentfrom monosodium glutamate production (Figure 9) [121]This is one of the largest treatment plants and is ten timeslarger than the largest plant built before in 2008 in ChinaAnother 11 ANAMMOXplants were implemented by Paquesseven of which are located in China (Table 5) As the worldrsquosbiggest developing market China contributes significantlytowards commercialization of ANAMMOX process

Besides imported technology some research groups inChina were set to operate with full scale ANAMMOXprocess with their own possessed sludge expertise andtechnology It came to know that ZhejiangUniversityANAM-MOX research group have succeeded in implementing twofull scale ANAMMOX treatment plants for treatment ofmonosodium glutamate wastewater (60m3) in Yiwu Cityand pharmaceutical wastewater (10m3) in Dongyang CityZhejiang Province China Some other research groups alsoopted to set up full scale application These initiatives are theclear indication that China already have achieved dramatic

progress in ANAMMOX research and very near to be one ofthe leading group in ANAMMOX technology

6 Conclusion

ANAMMOX process was considered to be one of the mostsustainable pathways for nitrogen removal from ammonium-rich wastewater During the past decades many Chinesegroups have dedicated their efforts on the ANAMMOXresearch The highest nitrogen removal rate in laboratoryscale has been obtained from a research group in Chinawhich is a strong evidence of development in ANAMMOXresearch Three new species of ANAMMOX bacteria havebeen identified among them two species are responsiblefor simultaneous ammonium and sulfate removal which isa new addition in ANAMMOX process for simultaneoustreatment Pilot-scale operations are expanding and usingdomestic expertise technology manpower and so forth fullscale application with domestic expertise and technology isbeckoning for commencement Overall Chinarsquos progress inANAMMOX process is appreciating and time befitting

61 Highlights Discovery of ANAMMOX and sulfate-dependent ANAMMOX bacteria ANAMMOX process andsulfate-dependent ANAMMOX process development forsimultaneous removal and pilot scale to full scale ANAM-MOX process application were reviewed

Conflict of Interests

The authors declare that there is no conflict of interests

Acknowledgments

The financial support of this work by the National NaturalScience Foundation of China (51204213) the Key Project


of Science and Technology program of Hunan Province(2013WK2007) the Special National Post-doctoral ScienceFoundation of China (2013T60782) the National Fundsfor Distinguished Young Scientists of China (50925417)the National Post-doctoral Science Foundation of China(2012M511769) and the Post-doctoral Foundation of CentralSouth University China is gratefully acknowledged Theauthors also want to appreciate the anonymous reviewers andeditor for their pertinent contribution to improve the paper

References

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[2] M Strous J J Heijnen J G Kuenen and M S M Jetten ldquoThesequencing batch reactor as a powerful tool for the study ofslowly growing anaerobic ammonium-oxidizing microorgan-ismsrdquoAppliedMicrobiology and Biotechnology vol 50 no 5 pp589ndash596 1998

[3] WR L van der StarW R AbmaD Blommers et al ldquoStartup ofreactors for anoxic ammonium oxidation experiences from thefirst full-scale anammox reactor in RotterdamrdquoWater Researchvol 41 no 18 pp 4149ndash4163 2007

[4] M S M Jetten S Logemann G Muyzer et al ldquoNovelprinciples in the microbial conversion of nitrogen compoundsrdquoAntonie van Leeuwenhoek International Journal of General andMolecular Microbiology vol 71 no 1-2 pp 75ndash93 1997

[5] B Kartal J G Kuenen and M C M van Loosdrecht ldquoSewagetreatment with anammoxrdquo Science vol 328 no 5979 pp 702ndash703 2010

[6] M Strous J A Fuerst E H M Kramer et al ldquoMissinglithotroph identified as new planctomyceterdquo Nature vol 400no 6743 pp 446ndash449 1999

[7] Y Tao D-W Gao Y Fu W-M Wu and N-Q Ren ldquoImpactof reactor configuration on anammox process start-up MBRversus SBRrdquo Bioresource Technology vol 104 pp 73ndash80 2012

[8] I Tsushima YOgasawara T Kindaichi H Satoh and SOkabeldquoDevelopment of high-rate anaerobic ammonium-oxidizing(anammox) biofilm reactorsrdquoWater Research vol 41 no 8 pp1623ndash1634 2007

[9] K Isaka Y Date T Sumino S Yoshie and S Tsuneda ldquoGrowthcharacteristic of anaerobic ammonium-oxidizing bacteria in ananaerobic biological filtrated reactorrdquo Applied Microbiology andBiotechnology vol 70 no 1 pp 47ndash52 2006

[10] I Fernandez J R Vazquez-Padın A Mosquera-Corral J LCampos and R Mendez ldquoBiofilm and granular systems toimprove Anammox biomass retentionrdquo Biochemical Engineer-ing Journal vol 42 no 3 pp 308ndash313 2008

[11] H Lopez S Puig R Ganigue M Ruscalleda M D Balaguerand J Colprim ldquoStart-up and enrichment of a granular anam-mox SBR to treat high nitrogen load wastewatersrdquo Journal ofChemical Technology and Biotechnology vol 83 no 3 pp 233ndash241 2008

[12] B-L Hu L-D Shen X-Y Xu and P Zheng ldquoAnaerobic ammo-nium oxidation (anammox) in different natural ecosystemsrdquoBiochemical Society Transactions vol 39 no 6 pp 1811ndash18162011

[13] B-L Hu P Zheng C-J Tang et al ldquoIdentification and quantifi-cation of anammox bacteria in eight nitrogen removal reactorsrdquoWater Research vol 44 no 17 pp 5014ndash5020 2010

[14] S Liu F Yang Z Gong et al ldquoApplication of anaero-bic ammonium-oxidizing consortium to achieve completelyautotrophic ammonium and sulfate removalrdquo Bioresource Tech-nology vol 99 no 15 pp 6817ndash6825 2008

[15] J Cai J X Jiang and P Zheng ldquoIsolation and identificationof bacteria responsible for simultaneous anaerobic ammoniumand sulfate removalrdquo Science China Chemistry vol 53 no 3 pp645ndash650 2010

[16] B L Hu P Zheng Q Mahmood H F Qian and D LWu ldquoCultivation granulation and characteristics of anaerobicammonium-oxidizing sludge in sequencing batch reactorrdquoWater Science and Technology vol 6 no 6 pp 71ndash79 2006

[17] B Kartal L van Niftrik J Rattray et al ldquoCandidatus ldquoBrocadiafulgidardquo an autofluorescent anaerobic ammonium oxidizingbacteriumrdquo FEMS Microbiology Ecology vol 63 no 1 pp 46ndash55 2008

[18] K Pynaert B F Smets S Wyffels D Beheydt S D Sicil-iano and W Verstraete ldquoCharacterization of an autotrophicnitrogen-removing biofilm from a highly loaded lab-scale rotat-ing biological contactorrdquo Applied and Environmental Microbiol-ogy vol 69 no 6 pp 3626ndash3635 2003

[19] M Schmid U Twachtmann M Klein et al ldquoMolecularevidence for genus level diversity of bacteria capable of catalyz-ing anaerobic ammonium oxidationrdquo Systematic and AppliedMicrobiology vol 23 no 1 pp 93ndash106 2000

[20] R-C Jin P Zheng A-H Hu Q Mahmood B-L Hu and GJilani ldquoPerformance comparison of two anammox reactors SBRand UBFrdquo Chemical Engineering Journal vol 138 no 1ndash3 pp224ndash230 2008

[21] P Zheng F-M Lin B-L Hu and J-S Chen ldquoStart-up of anaer-obic ammonia oxidation bioreactor with nitrifying activatedsludgerdquo Journal of Environmental Sciences vol 16 no 1 pp 13ndash16 2004

[22] C Trigo J L Campos J M Garrido and R Mendez ldquoStart-upof the Anammox process in a membrane bioreactorrdquo Journal ofBiotechnology vol 126 no 4 pp 475ndash487 2006

[23] A O Sliekers K A Third W Abma J G Kuenen and M SM Jetten ldquoCANON and Anammox in a gas-lift reactorrdquo FEMSMicrobiology Letters vol 218 no 2 pp 339ndash344 2003

[24] U Imajo T Tokutomi and K Furukawa ldquoGranulation ofAnammox microorganisms in up-flow reactorsrdquoWater Scienceand Technology vol 49 no 5-6 pp 155ndash163 2004

[25] K Isaka T Sumino and S Tsuneda ldquoHigh nitrogen removalperformance at moderately low temperature utilizing anaerobicammonium oxidation reactionsrdquo Journal of Bioscience andBioengineering vol 103 no 5 pp 486ndash490 2007

[26] C-J Tang P Zheng andQMahmood ldquoThe shear force amend-ments on the slugging behavior of upflow Anammox granularsludge bed reactorrdquo Separation and Purification Technology vol69 no 3 pp 262ndash268 2009

[27] H Li S Zhou W Ma G Huang and B Xu ldquoFast start-up ofANAMMOX reactor operational strategy and some character-istics as indicators of reactor performancerdquo Desalination vol286 pp 436ndash441 2012

[28] C-J Tang P Zheng C-H Wang et al ldquoPerformance ofhigh-loaded ANAMMOX UASB reactors containing granularsludgerdquoWater Research vol 45 no 1 pp 135ndash144 2011


[29] T Chen P Zheng C Tang SWang and S Ding ldquoPerformanceof ANAMMOX-EGSB reactorrdquo Desalination vol 278 no 1ndash3pp 281ndash287 2011

[30] T Chen P Zheng L Shen S Ding and Q Mahmood ldquoKineticcharacteristics and microbial community of Anammox-EGSBreactorrdquo Journal of Hazardous Materials vol 190 no 1ndash3 pp28ndash35 2011

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[32] YQMiuTheory andTechnology ofWastewaterDesulfurizationChemical Industry Press Beijing China 2004

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[35] L X Dong Y T Lu Q Y Han and Z Y Wang ldquoThe effectof sulfate reduction on ammonium oxidation and its inhibitorypropertiesrdquo Journal of XirsquoAn University of Architecture AndTechnology vol 38 no 3 pp 425ndash428 2006

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[37] L Zhang P Zheng Y He and R Jin ldquoPerformance of sulfate-dependent anaerobic ammonium oxidationrdquo Science in ChinaB vol 52 no 1 pp 86ndash92 2009

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[39] R C Jin G F Yang Q Q Zhang C Ma J J Yu and B S XingldquoThe effect of sulfide inhibition on the ANAMMOX processrdquoWater Research vol 47 no 3 pp 1459ndash1469 2013

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[44] M C M van Loosdrecht ldquoEnvironmental Biotechnologistwins Lee Kuan Yew Water Prize 2012rdquo Fact Sheet 2012httpwwwsiwwcomsgmediaenvironmental-biotechnolo-gist-wins-lee-kuan-yew-water-prize-2012

[45] M Schmid K Walsh R Webb et al ldquoCandidatus ldquoScalinduabrodaerdquo sp nov Candidatus ldquoScalindua wagnerirdquo sp nov TwoNew Species of Anaerobic Ammonium Oxidizing BacteriardquoSystematic and AppliedMicrobiology vol 26 no 4 pp 529ndash5382003

[46] B Kartal J Rattray L A van Niftrik et al ldquoCandidatusldquoAnammoxoglobus propionicusrdquo a new propionate oxidizingspecies of anaerobic ammonium oxidizing bacteriardquo Systematicand Applied Microbiology vol 30 no 1 pp 39ndash49 2007

[47] Z-X Quan S-K Rhee J-E Zuo et al ldquoDiversity ofammonium-oxidizing bacteria in a granular sludge anaero-bic ammonium-oxidizing (anammox) reactorrdquo EnvironmentalMicrobiology vol 10 no 11 pp 3130ndash3139 2008

[48] M M M Kuypers G Lavik D Woebken et al ldquoMassivenitrogen loss from the Benguela upwelling system throughanaerobic ammonium oxidationrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 102 no18 pp 6478ndash6483 2005

[49] M C Schmid N Risgaard-Petersen J van de Vossenberg et alldquoAnaerobic ammonium-oxidizing bacteria in marine environ-ments widespread occurrence but lowdiversityrdquoEnvironmentalMicrobiology vol 9 no 6 pp 1476ndash1484 2007

[50] C R Penton AHDevol and JM Tiedje ldquoMolecular evidencefor the broad distribution of anaerobic ammonium-oxidizingbacteria in freshwater and marine sedimentsrdquo Applied andEnvironmental Microbiology vol 72 no 10 pp 6829ndash68322006

[51] B Kartal M Koleva R Arsov W van der Star M S M Jettenand M Strous ldquoAdaptation of a freshwater anammox popula-tion to high salinity wastewaterrdquo Journal of Biotechnology vol126 no 4 pp 546ndash553 2006

[52] K Windey I de Bo and W Verstraete ldquoOxygen-limitedautotrophic nitrification-denitrification (OLAND) in a rotatingbiological contactor treating high-salinity wastewaterrdquo WaterResearch vol 39 no 18 pp 4512ndash4520 2005

[53] P Han and J D Gu ldquoMore refined diversity of anammoxbacteria recovered and distribution in different ecosystemsrdquoApplied Microbiology and Biotechnology vol 97 pp 3653ndash36632013

[54] Y-G Hong M Li H Cao and J-D Gu ldquoResidence ofhabitat-specific anammox bacteria in the deep-sea subsurfacesediments of the south china sea analyses of marker gene abun-dance with physical chemical parametersrdquo Microbial Ecologyvol 62 no 1 pp 36ndash47 2011

[55] H Dang R Chen L Wang et al ldquoEnvironmental factors shapesediment anammox bacterial communities in hypernutrifiedJiaozhou Bay Chinardquo Applied and Environmental Microbiologyvol 76 no 21 pp 7036ndash7047 2010

[56] H Li S Chen B-Z Mu and J-D Gu ldquoMolecular detection ofanaerobic ammonium-oxidizing (Anammox) bacteria in high-temperature petroleum reservoirsrdquo Microbial Ecology vol 60no 4 pp 771ndash783 2010

[57] G Zhu S Wang YWang et al ldquoAnaerobic ammonia oxidationin a fertilized paddy soilrdquo International Society for MicrobialEcology vol 5 no 12 pp 1905ndash1912 2011

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monosodium glutamate industrial wastewater treatment sys-temrdquo Journal of Hazardous Materials vol 199-200 pp 193ndash1992012

[60] J Wang and J-D Gu ldquoDominance of Candidatus Scalinduaspecies in anammox community revealed in soils with differentduration of rice paddy cultivation in Northeast Chinardquo AppliedMicrobiology and Biotechnology vol 97 no 4 pp 1785ndash17982013

[61] M Li and J-D Gu ldquoAdvances in methods for detection ofanaerobic ammonium oxidizing (anammox) bacteriardquo AppliedMicrobiology and Biotechnology vol 90 no 4 pp 1241ndash12522011

[62] S Liu L D Shen L Lou G Tian P Zheng and B L HuldquoSpatial distribution and factors shaping the niche segregationof Ammonia-oxidizing microorganisms in the Qiantang riverChinardquoApplied and Environmental Microbiology vol 79 no 13pp 4065ndash4071 2013

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[65] H L Baolan S Liu L D Shen P Zheng X Y Xu andL P Lou ldquoEffect of different Ammonia concentrations oncommunity succession of Ammonia-oxidizingmicroorganismsin a simulated paddy soil columnrdquo PloS One vol 7 no 8 ArticleID e44122 2012

[66] B Hu L Shen P Du P Zheng X Xu and J Zeng ldquoTheinfluence of intense chemical pollution on the communitycomposition diversity and abundance of anammox bacteria inthe Jiaojiang Estuary (China)rdquo PLoS ONE vol 7 no 3 ArticleID e33826 2012

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[68] M Li H Cao Y-G Hong and J D Gu ldquoSeasonal dynamics ofanammox bacteria in estuarial sediment of the mai po naturereserve revealed by analyzing the 16s rRNA and hydrazineoxidoreductase (hzo) genesrdquo Microbes and Environments vol26 no 1 pp 15ndash22 2011

[69] Y Wang G Zhu H R Harhangi et al ldquoCo-occurrence anddistribution of nitriteminusdependent anaerobic ammonium andmethane-oxidizing bacteria in a paddy soilrdquoFEMSMicrobiologyLetters vol 336 no 2 pp 79ndash88 2012

[70] L D Shen B L Hu P Zheng et al ldquoMolecular detection ofanammox bacteria in the sediment ofWest LakerdquoActa ScientiaeCircumstantiae vol 31 no 8 pp 1609ndash1615 2011

[71] R-C Jin and P Zheng ldquoKinetics of nitrogen removal in highrate anammox upflow filterrdquo Journal of Hazardous Materialsvol 170 no 2-3 pp 652ndash656 2009

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[73] R-C Jin P Zheng Q Mahmood and L Zhang ldquoPerformanceof a nitrifying airlift reactor using granular sludgerdquo Separationand Purification Technology vol 63 no 3 pp 670ndash675 2008

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Anammox UBFrdquo Bioresource Technology vol 101 no 8 pp2700ndash2705 2010

[75] Y Yuan Y Huang H Deng Y Li and Y Pan ldquoResearch onenrichment for anammox bacteria inoculated via enhancedendogenous denitrificationrdquo in Life System Modeling and Intel-ligent Computing vol 6330 pp 700ndash707 Springer BerlinGermany 2010

[76] D Liao X Li Q Yang G Zeng L Guo and X Yue ldquoEffect ofinorganic carbon on anaerobic ammonium oxidation enrichedin sequencing batch reactorrdquo Journal of Environmental Sciencesvol 20 no 8 pp 940ndash944 2008

[77] T Wang H Zhang D Gao et al ldquoEnrichment of Anammoxbacteria in seed sludges from different wastewater treatingprocesses and start-up of Anammox processrdquoDesalination vol271 no 1ndash3 pp 193ndash198 2011

[78] S-Q Ni B-Y Gao C-C Wang J-G Lin and S Sung ldquoFaststart-up performance and microbial community in a pilot-scale anammox reactor seeded with exotic mature granulesrdquoBioresource Technology vol 102 no 3 pp 2448ndash2454 2011

[79] S Bagchi R Biswas and T Nandy ldquoStart-up and stabilizationof an Anammox process from a non-acclimatized sludge inCSTRrdquo Journal of Industrial Microbiology and Biotechnologyvol 37 no 9 pp 943ndash952 2010

[80] T Wang H Zhang F Yang S Liu Z Fu and H Chen ldquoStart-up of the Anammox process from the conventional activatedsludge in a membrane bioreactorrdquo Bioresource Technology vol100 no 9 pp 2501ndash2506 2009

[81] C-J Tang P Zheng Q Mahmood and J-W Chen ldquoStart-upand inhibition analysis of the Anammox process seeded withanaerobic granular sludgerdquo Journal of Industrial Microbiologyand Biotechnology vol 36 no 8 pp 1093ndash1100 2009

[82] U van Dongen M S M Jetten and M C M van LoosdrechtldquoThe SHARON-Anammox process for treatment of ammoniumrichwastewaterrdquoWater Science andTechnology vol 44 no 1 pp153ndash160 2001

[83] W S H R H Petrucci and F G Herring General ChemistryPrinciples and Modern Applications Higher Education PressBeijing China 8th edition 2004

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[85] Q Mahmood Process performance optimization and micro-biology of anoxic sulfide biooxidation using nitrite as electronacceptor [PhD Dissertation] Zhejiang University HangzhouChina 2007

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[87] G F Yang Q Q Zhang and R C Jin ldquoChanges in the nitrogenremoval performance and the properties of granular sludgein an Anammox system under oxytetracycline (OTC) stressrdquoBioresource Technology vol 129 pp 65ndash71 2013

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[89] H F Lu Q X Ji S Ding and P Zheng ldquoThemorphological andsettling properties of ANAMMOX granular sludge in high-ratereactorsrdquo Bioresource Technology vol 143 pp 592ndash597 2013


[90] A Franco E Roca and J M Lema ldquoGranulation in high-loaddenitrifying upflow sludge bed (USB) pulsed reactorsrdquo WaterResearch vol 40 no 5 pp 871ndash880 2006

[91] K Z Su B J Ni and H Q Yu ldquoModeling and optimizationof granulation process of activated sludge in sequencing batchreactorsrdquo Biotechnology and Bioengineering vol 110 pp 1312ndash1322 2013

[92] H F Lu P Zheng Q X Ji et al ldquoThe structure density andsettlability of anammox granular sludge in high-rate reactorsrdquoBioresource Technology vol 123 pp 312ndash317 2012

[93] M S M Jetten M Wagner J Fuerst M van Loosdrecht GKuenen and M Strous ldquoMicrobiology and application of theanaerobic ammonium oxidation (lsquoanammoxrsquo) processrdquo CurrentOpinion in Biotechnology vol 12 no 3 pp 283ndash288 2001

[94] A A van de Graaf P de Bruijn L A Robertson M S MJetten and J G Kuenen ldquoAutotrophic growth of anaerobicammonium-oxidizingmicro-organisms in a fluidized bed reac-torrdquoMicrobiology vol 142 no 8 pp 2187ndash2196 1996

[95] L van Niftrik W J C Geerts E G van Donselaar et alldquoCombined structural and chemical analysis of the anammoxo-some a membrane-bounded intracytoplasmic compartment inanammox bacteriardquo Journal of Structural Biology vol 161 no 3pp 401ndash410 2008

[96] Y Liu and J-H Tay ldquoThe essential role of hydrodynamic shearforce in the formation of biofilm and granular sludgerdquo WaterResearch vol 36 no 7 pp 1653ndash1665 2002

[97] L W Hulshoff Pol S I de Castro Lopes G Lettinga and P NL Lens ldquoAnaerobic sludge granulationrdquoWater Research vol 38no 6 pp 1376ndash1389 2004

[98] X-W Liu G-P Sheng andH-Q Yu ldquoPhysicochemical charac-teristics of microbial granulesrdquo Biotechnology Advances vol 27no 6 pp 1061ndash1070 2009

[99] Y-Q Liu Y Liu and J-H Tay ldquoThe effects of extracellular poly-meric substances on the formation and stability of biogranulesrdquoApplied Microbiology and Biotechnology vol 65 no 2 pp 143ndash148 2004

[100] J Quarmby and C F Forster ldquoAn examination of the structureof UASB granulesrdquo Water Research vol 29 no 11 pp 2449ndash2454 1995

[101] F M Cuervo-Lopez F Martinez M Gutierrez-Rojas R ANoyola and J Gomez ldquoEffect of nitrogen loading rate and car-bon source on denitrification and sludge settleability in upflowanaerobic sludge blanket (UASB) reactorsrdquo Water Science andTechnology vol 40 no 8 pp 123ndash130 1999

[102] D J Batstone and J Keller ldquoVariation of bulk properties ofanaerobic granules with wastewater typerdquo Water Research vol35 no 7 pp 1723ndash1729 2001

[103] F O Martınez J Lema R Mendez F Cuervo-Lopez and JGomez ldquoRole of exopolymeric protein on the settleability ofnitrifying sludgesrdquo Bioresource Technology vol 94 no 1 pp 43ndash48 2004

[104] J Wu H-M Zhou H-Z Li P-C Zhang and J Jiang ldquoImpactsof hydrodynamic shear force on nucleation of flocculent sludgein anaerobic reactorrdquoWater Research vol 43 no 12 pp 3029ndash3036 2009

[105] M S M Jetten L V Niftrik M Strous B Kartal J T Keltjensand H J M Op Den Camp ldquoBiochemistry and molecularbiology of anammox bacteria biochemistry and molecularbiology of anammox bacteria MSM Jetten et alrdquo CriticalReviews in Biochemistry and Molecular Biology vol 44 no 2-3 pp 65ndash84 2009

[106] M G Klotz M C Schmid M Strous H J M Op Den CampM S M Jetten and A B Hooper ldquoEvolution of an octahaemcytochrome c protein family that is key to aerobic and anaerobicammonia oxidation by bacteriardquo Environmental Microbiologyvol 10 no 11 pp 3150ndash3163 2008

[107] M C Schmid A B Hooper M G Klotz et al ldquoEnvironmentaldetection of octahaem cytochrome c hydroxylaminehydrazineoxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteriardquo Environmental Microbiology vol 10 no 11pp 3140ndash3149 2008

[108] T T Chen P Zheng and L D Shen ldquoGrowth and metabolismcharacteristics of anaerobic ammonium-oxidizing bacteriaaggregatesrdquoAppliedMicrobiology and Biotechnology vol 97 no12 pp 5575ndash5583 2013

[109] J D Bryers and F Drummond ldquoLocal macromolecule diffusioncoefficients in structurally non-uniformbacterial biofilms usingfluorescence recovery after photobleaching (FRAP)rdquo Biotech-nology and Bioengineering vol 60 no 4 pp 462ndash473 1998

[110] D de Beer P Stoodley and Z Lewandowski ldquoMeasurementof local diffusion coefficients in biofilms by microinjection andconfocalmicroscopyrdquoBiotechnology and Bioengineering vol 53no 2 pp 151ndash158 1997

[111] L W Hulshoff Pol W J de Zeeuw C T M Velzeboer andG Lettinga ldquoGranulation in UASB-reactorsrdquoWater Science andTechnology vol 15 no 8-9 pp 291ndash304 1983

[112] L Tijhuis B Hijman M C M van Loosdrecht and J J Hei-jnen ldquoInfluence of detachment substrate loading and reactorscale on the formation of biofilms in airlift reactorsrdquo AppliedMicrobiology and Biotechnology vol 45 no 1-2 pp 7ndash17 1996

[113] J Chen Q Ji P Zheng T Chen C Wang and Q MahmoodldquoFloatation and control of granular sludge in a high-rate anam-mox reactorrdquoWater Research vol 44 no 11 pp 3321ndash3328 2010

[114] A Dapena-Mora J L Campos A Mosquera-Corral M S MJetten and R Mendez ldquoStability of the ANAMMOX process ina gas-lift reactor and a SBRrdquo Journal of Biotechnology vol 110no 2 pp 159ndash170 2004

[115] A Dapena-Mora B Arrojo J L Campos A Mosquera-Corraland R Mendez ldquoImprovement of the settling properties ofAnammox sludge in an SBRrdquo Journal of Chemical Technologyand Biotechnology vol 79 no 12 pp 1417ndash1420 2004

[116] Y Ma D Hira Z Li C Chen and K Furukawa ldquoNitrogenremoval performance of a hybrid anammox reactorrdquo Biore-source Technology vol 102 no 12 pp 6650ndash6656 2011

[117] P An X Xu F Yang L Liu and S Liu ldquoA pilot-scale study onnitrogen removal from dry-spun acrylic fiber wastewater usinganammox processrdquo Chemical Engineering Journal vol 222 pp32ndash40 2013

[118] D D Ebbing and S D GammonGeneral Chemistry HoughtonMifflin Boston MA USA 9th edition 2007

[119] C Tang P Zheng J Chen X Chen S Zhou and G DingldquoStart-up and process control of a pilot-scale Anammox biore-actor at ambient temperaturerdquoChinese Journal of Biotechnologyvol 25 no 3 pp 406ndash412 2009

[120] S-Q Ni S Sung Q-Y Yue and B-Y Gao ldquoSubstrate removalevaluation of granular anammox process in a pilot-scale upflowanaerobic sludge blanket reactorrdquo Ecological Engineering vol38 no 1 pp 30ndash36 2012

[121] W Driessen and G Reitsma ldquoOne-Step ANAMMOX Process-Water Projects Onlinerdquo UKWater Project 2011

Submit your manuscripts athttpwwwhindawicom

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Microbiology


[14] and Bacillus benzoevorans [15] have been discoveredin China which are the functional community to removeammonium and sulfate simultaneously

High rate is one of the prime objectives for ANAMMOXprocess Within the last decades some specialized reactorsystems such as sequencing batch reactor (SBR) [2 16ndash19] rotating biological contactor (RBC) [18] trickling filter[19] UBF reactor [20] granular sludge bed reactor [21]and membrane bioreactor [3 22] have been introduced inboth laboratory and full scale to obtain high removal rateand finally noticed that these reactors played an importantrole in securing high rate performance for ammonium andnitrite removal The NRR of conventional nitrogen removalbiotechnologies was less than 05 kg-Nm3d [20] while forANAMMOX process it was higher than 5 kg-Nm3d asobtained by a number of researchers using different reactorssuch as upflow biofilter upflow anaerobic sludge blanket(UASB) reactor and gas-lift reactor [3 23ndash26]

Nitrogen pollution (N-pollution) causes serious environ-mental problems N-pollution not only hampers the sustain-able development of agriculture fishery tourism and so forthbut also threatens the living environment of human beingsAccording to the report of ldquothe state of the environmentin China (2009)rdquo the ammonium emission was up to 123million tons per year [27] Thus it was necessary to removenitrogen from different ammonium wastewater in ChinaTo fulfill the demand the research groups in China startedto carry out ANAMMOX research and obtained significantoutcomes As a part of continuation of ANAMMOX researchnitrogen removal rate higher than 10 kg-Nm3dwas obtainedby a significant number of researchers in China [26 28ndash30] Till now the highest NRR in the world was reportedby Chinese research group which was 743ndash767 kg-Nm3dat hydraulic retention time (HRT) of 016 h [28] Besidesnitrogen sulfur is another necessary nutrient for all livingcreatures which means that no one can grow and reproducewithout them [31 32] Ammonium and sulfate are coexistentin seawater and sediments with the average concentrations of100mMand 20mM respectively and this coexistence offers abasic condition for sulfate-dependent anaerobic ammoniumoxidation [33] Using this basic condition simultaneousremoval of ammonium and sulfate was discovered in 2001in an anaerobic fluidized-bed reactor by Fdz-Polanco etal [34] and they reported that 80 sulfate was convertedto elemental sulfur accompanied by ammonium oxidationto dinitrogen gas Subsequently the existence of sulfate-dependent anaerobic ammonium oxidation has been con-firmed by other researchers [14 35ndash38] Sulfate-dependentANAMMOX process was also reported by a number ofresearchers in China [14 15 37ndash39]

The research groups from the mainland Taiwan andHong Kong of China have conducted a lot of investigationson ANAMMOX process including density and settleabilitymechanism of sludge modeling of packing pattern controlmechanism for floating sludge sequential biocatalyst addi-tion for inhibition recovery process recovery mechanismsillustration and so on to enhance the ANAMMOX processperformance and stability of the process After nearly 20

years of hard work the full-scale application of the ANAM-MOX has been successfully implemented for treatment ofmonosodium glutamate wastewater pharmaceutical wastew-ater and landfill leachate [40ndash44] A series of progress in bac-teria and process development were also forwarded whichcontributed significantly to help us understand the processand finally instigated researchers to operate and control thenovel autotrophic process The objective of this review isto present a detailed comparative summary of previous andcurrent researches on the progress in ANAMMOX bacteriadiscovery process development and the full-scale applicationin China

2 Recent Progress of ANAMMOX Bacteriain China

The ANAMMOX process is carried out by a group ofANAMMOX bacteria which are monophyletic group ofbacteria under Planctomycetes phylum Brocadiales orderand Candidatus taxonomic component [12] Till now at least5 genera and 13 species have been identified using culture-independentmolecular techniques [12] includingCandidatusldquoBrocadiardquo (Ca ldquoBrocadia anammoxidansrdquo Ca ldquoBrocadiafulgidardquo and Ca ldquoBrocadia sinicardquo) Candidatus ldquoKuene-nia stuttgartiensisrdquo Candidatus ldquoScalinduardquo (Ca ldquoScalinduabrodaerdquo Ca ldquoScalindua wagnerirdquo Ca ldquoScalindua sorokiniirdquoCa ldquoScalindua arabicardquo Ca ldquoScalindua sinooilfieldrdquo and CaldquoScalindua zhengheirdquo) Candidatus ldquoAnammoxoglobusrdquo (CaldquoAnammoxoglobus propionicusrdquo and Ca ldquoAnammoxoglobussulfaterdquo) Candidatus ldquoJettenia asiaticardquo

Candidatus Brocadia Kuenenia Scalindua Anammox-oglobus Jettenia genera have been isolated from differentwastewater treatment systems [6 17 19 45ndash47] only onegenus (Candidatus Scalindua) seems to be predominant inmarine ecosystems ranging from arctic to tropical regions[48ndash50] K stuttgartiensis is fresh water ANAMMOX bac-terium but could adapt to high salinity (up to 3) [51]Addition of organic acids like propionate or acetate favoredto proliferate the Brocadia fulgida or Anammoxoglobuspropionicus species with low fluxes of organicmatter [17 46]

Three new species of ANAMMOX bacteria (Candida-tus Brocadia sinica Candidatus Anammoxoglobus sulfateand Bacillus benzoevorans) have been discovered in ChinaAmong these three species Candidatus Brocadia sinica wasisolated from ANAMMOX reactors and other two species(Anammoxoglobus sulfate and Bacillus benzoevorans) wereidentified in sulfate removal reactors

21 Candidatus Brocadia sinica Hu et al [13] operated 8bioreactors with highly compact granulated sludge in dif-ferent physicochemical conditions Although the reactorswere operated in distinct variations in temperature (9ndash27∘C) or influent wastewater (inorganic medium glucoseor glutamate addition) these variations did not influencethe inhibition of ANAMMOX bacteria in reactor Vice-versathese changing conditions play an important role to grow uplarge population of the species which only can adapt to thischanging situation Especially a new ANAMMOX bacterial


(a) (b) (c) (d) (e)










4Cl(NH

4)2SO4and NaNO




4ndashN NO































4


4


4













4

2minus andNH4


4



4

+ + SO4


2O


4

+ndashN and SO4

2minus


2[84] This higher








3SO4

2minus+ 4NH

4

+997888rarr 3S

2

minus+ 4NO

2

minus+ 4H2O + 8H+


3S2

minus+ 2NO

2


2+ 3S + 4H

2O


2NO2

minus+ 2NH

4

+997888rarr 2N

2+ 4H2O


3S2

minus+ 4NO

2


4


2

(4)

NH4

++

1

2

SO4

2minus997888rarr

1

2

N2+

1

2

S + 2H2O (5)



4)2SO4and












Table3Overviewof

thes

ulfate-dependent


ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


(a) (b) (c) (d) (e)










4Cl(NH

4)2SO4and NaNO




4ndashN NO































4


4


4













4

2minus andNH4


4



4

+ + SO4


2O


4

+ndashN and SO4

2minus


2[84] This higher








3SO4

2minus+ 4NH

4

+997888rarr 3S

2

minus+ 4NO

2

minus+ 4H2O + 8H+


3S2

minus+ 2NO

2


2+ 3S + 4H

2O


2NO2

minus+ 2NH

4

+997888rarr 2N

2+ 4H2O


3S2

minus+ 4NO

2


4


2

(4)

NH4

++

1

2

SO4

2minus997888rarr

1

2

N2+

1

2

S + 2H2O (5)



4)2SO4and












Table3Overviewof

thes

ulfate-dependent


ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






























4


4


4













4

2minus andNH4


4



4

+ + SO4


2O


4

+ndashN and SO4

2minus


2[84] This higher








3SO4

2minus+ 4NH

4

+997888rarr 3S

2

minus+ 4NO

2

minus+ 4H2O + 8H+


3S2

minus+ 2NO

2


2+ 3S + 4H

2O


2NO2

minus+ 2NH

4

+997888rarr 2N

2+ 4H2O


3S2

minus+ 4NO

2


4


2

(4)

NH4

++

1

2

SO4

2minus997888rarr

1

2

N2+

1

2

S + 2H2O (5)



4)2SO4and












Table3Overviewof

thes

ulfate-dependent


ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology












4

2minus andNH4


4



4

+ + SO4


2O


4

+ndashN and SO4

2minus


2[84] This higher








3SO4

2minus+ 4NH

4

+997888rarr 3S

2

minus+ 4NO

2

minus+ 4H2O + 8H+


3S2

minus+ 2NO

2


2+ 3S + 4H

2O


2NO2

minus+ 2NH

4

+997888rarr 2N

2+ 4H2O


3S2

minus+ 4NO

2


4


2

(4)

NH4

++

1

2

SO4

2minus997888rarr

1

2

N2+

1

2

S + 2H2O (5)



4)2SO4and












Table3Overviewof

thes

ulfate-dependent


ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






3SO4

2minus+ 4NH

4

+997888rarr 3S

2

minus+ 4NO

2

minus+ 4H2O + 8H+


3S2

minus+ 2NO

2


2+ 3S + 4H

2O


2NO2

minus+ 2NH

4

+997888rarr 2N

2+ 4H2O


3S2

minus+ 4NO

2


4


2

(4)

NH4

++

1

2

SO4

2minus997888rarr

1

2

N2+

1

2

S + 2H2O (5)



4)2SO4and












Table3Overviewof

thes

ulfate-dependent


ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table3Overviewof

thes

ulfate-dependent


ationin

China

Source

pHRe

actor

VSSgL

HRT

Influ

entm

gL

Removalratio

Averager

emovaleffi

ciency

()

Reference

NH

4ndashN

SO4ndashS

NH

4SO

4NH

4ndashN

SO4ndashS

K 2SO

485

Lab-scaler

eactor

NA

1d229

163

2011

444

40[15]

NH

4Cl

NaN

O2

8ndash82

NRB

Creactor

032ndash0

054

4ndash24

h288b

NA

17117

550

bNA

[14]

(NH

4)2SO

4(N

H4)

2SO

4NH

4Cl

75ndash85

UASB

reactor

NA

15d

60240

21

4030

[38]

NaN

O2

NaSO

4(N

H4)

2SO

475

Expand

edbedreactor

149

1d843

130

21

5682a

7167a

[37]

NaN

O2

Na 2Ssdot9H

2O833plusmn018

UASB

reactor

357

08h

350

264

NA

947

NA

[39]

a Con

centratio

nin

mgL

b con

centratio

nin

mmolLD

NAno

tAvailable


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


















(a) (b)












(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



(a)


(b)








ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


ANAMMOX sludge

(a)


(b)











+ and NO2





(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



(n)

(h)

(g)

(e)

(j)

(c)

(b)

(a)

(m)

(l)

(k)

(f)

(d)

(i)





Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




Aggregation


ANAMMOX bacteria


Composite


GranuleGrow-up













Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Floatation



Settle down

Gas pocketbreak

Wash out

(a)

E F

DC

BA

(b)










(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


(a) (b)






119877 = 0527119862119883119902(1 minus

119862119883

120588 granule)

250

(

119862119883


016

119862023

(6)



119883is equal to


119883was



119883







Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table4Briefd

escriptio

nof

pilot-s

caleapplicationof

ANAMMOXprocessinCh

ina

Wastewater

Reactor

Working

volume

VSSgL

pHTemp∘C

Influ

entm

gL

Ratio

Removaleffi

ciency

()

NRR

kgm

3 dRe

ference

NH

4ndashN

NO

2ndashN

NH

4N

O2

NH

4ndashN

NO

2ndashN

Synthetic

wastewater

UASB

25m

3435

68

5ndash27

299

336

1112

8498

130

[119]

Synthetic

wastewater

UASB

reactor

50L

378

75ndash80

3744

8575

11plusmn026

9399

278

[78]

DAFW

UASB

reactor

68L

22

68ndash7035plusmn1

150ndash

180

120ndash

150

112

685

90NA

[117]

Synthetic

wastewater

UASB

reactor

20L

7275

ndash80

35377

557

11

855

914

640T

N[120]

PWMABR

reactor

225m

310

72ndash85

12ndash26

NA

NA

NA

98NA

NA

[42]

DAFW

dry-spu

nacrylic

fiber

wastewaterP

Wpharm

aceuticalwasteN

Ano

tavailable









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology









Paque [44]









6 Conclusion





Acknowledgments




References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



References






































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology










































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Review Article The Increasing Interest of ANAMMOX...

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