Biotechnological Potential Aquatic Plant Microbe Interactions COB2010

Available online at www.sciencedirect.com

Biotechnological potential of aquatic plant–microbe interactionsL Stout1 and K Nusslein2

The rhizosphere in terrestrial systems is the region of soil

surrounding plant roots where there is increased microbial

activity; in aquatic plants, this definition may be less clear

because of diffusion of nutrients in water, but there is still a zone

of influence by plant roots in this environment [1]. Within that

zone chemical conditions differ from those of the surrounding

environment as a consequence of a range of processes that

were induced either directly by the activity of plant roots or by

the activity of rhizosphere microflora. Recently, there are a

number of new studies related to rhizospheres of aquatic plants

and specifically their increased potential for remediation of

contaminants, especially remediation of metals through

aquatic plant–microbial interaction.

Addresses1 Department of Biology, Southern Connecticut State University,

New Haven, CT 06515, United States2 Department of Microbiology, University of Massachusetts, Amherst,

MA 01003-9298, United States

Corresponding authors: Stout, L ([email protected]) and

Nusslein, K ([email protected])

Current Opinion in Biotechnology 2010, 21:339–345

This review comes from a themed issue on

Environmental biotechnology

Edited by Sharon Borglin and John van der Meer

0958-1669/$ – see front matter

# 2010 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.copbio.2010.04.004

Application, advantages, and limitations ofplant-based remediationPhytoremediation, the use of plants and their associated

microbial communities to remove or inactivate pollutants

from the environment, includes any of several technol-

ogies for detoxifying the environment with genetically

modified or wild-type plants [2�]. Phytoremediation of

aquatic environments may be used as an alternative or in

addition to conventional remediation methods including

ion exchange resins and electrodialysis, chemical precipi-

tation, sedimentation, microfiltration, and reverse osmosis

[3��]. Biological remediation techniques offer effective

alternative treatments that are often less costly and are

considered more environmentally friendly and publicly

acceptable than conventional technologies.

Various phytoremediation technologies include phytoex-

traction, phytovolatilization, phytostabilization, and rhi-

www.sciencedirect.com

zofiltration and are summarized in several reviews

[4,5�,6��]. Recent studies have applied some of these

technologies to phytoremediation of heavy metals in

aquatic or wetland systems. For example, Murakami

et al. [7��] used rice cultivars that accumulated high levels

of cadmium to remove metal from contaminated paddy

fields. In these conditions where rice was well-adapted to

growth, one rice cultivar accumulated 10 times as much

Cd as Thlaspi caerulescens, a terrestrial plant well known for

its ability to accumulate heavy metals.

Rhizofiltration, the use of plants to remove heavy metals

from aqueous environments, has been extensively tested

as a way to remove contaminants from solutions, and can

include aquatic or terrestrial plants in hydroponic sys-

tems. Recently, sunflower and bean plants were tested for

their abilities to remove U from contaminated ground-

water. In laboratory batch experiments bean plants

removed more than 70% and sunflower removed more

than 80% of U but when sunflower was tested in a

continuous rhizofiltration system, U removal was greater

than 99% [8]. Aquatic and wetland plants including the

water hyacinth Eichhorinia crassipes [9,10�], the invasive

reed Phragmites australis [11�], the duckweeds Spirodelapolyrrhiza [12], Lemna minor [13�,14], and Lemna gibba[15,16], the aquatic fern Azolla pinnata [17�], and yellow

velvetleaf Limnocharis flava [18] have recently been stu-

died for their abilities to remove metals from aquatic

systems and show promising results. For instance, A.pinnata was found to remove as much as 94% of Hg from

a solution [17�], while Eichhornia crassipes was found to

accumulate Cr in its shoots at 223 times the concentration

in the water [9], and removed 84% of Cr from water and

95% of Zn from water [10�]. While metals negatively

affected growth of Lemna gibba, the plants were able to

remove 90% of Cd from solution after six to eight days

[16].

Metal tolerance and resistance: the bacterialsideBacteria have demonstrated elevated tolerance to metals

using many diverse mechanisms. They may maintain

metal homeostasis, keeping concentrations of essential

metals such as Zn from reaching toxic levels within cells

[19] or they may contain resistance systems, active mech-

anisms for removing or sequestering metals [20]. For

heavy metals including Cd, Zn, Ni, Cr, Co, and Cu, there

are several types of resistance systems, including efflux

pumps to remove metals from the cell, and sequestration

mechanisms to bind metal inside the cell. The two known

types of efflux systems are ATPases, which pump out

metals using ATP to drive the reaction, and proton


mailto:[email protected]

mailto:[email protected]

http://dx.doi.org/10.1016/j.copbio.2010.04.004

340 Environmental biotechnology

antiports, which use the proton gradient to pump metals

across the cell membrane [21]. Another mechanism of

bacterial metal resistance, best known in cyanobacteria, is

sequestration by metallothioneins. Metallothioneins bind

metals to sulfhydryl groups of cysteine residues [22,23].

Pages et al. recently described cadmium tolerance in

Stenotrophomonas maltophilia, and found not only a Cd

efflux pump but also accumulation of CdS particles [24].

Some bacteria expressing metal resistance produce more

extracellular polymeric substances (EPS), which bind the

metal, perhaps making the microenvironment around the

plant less toxic. Production of EPS has been shown to

increase with increased metal resistance [25��].

In different strains of Rhizobium leguminosarum, Cd toler-

ant strains showed increased levels of glutathione, indi-

cating that this tripeptide allows the bacterium to deal

with heavy metals, rather than an efflux system [26]. The

biomarker glutathione is an important antioxidant that

may protect against metal toxicity associated with oxi-

dative stress. Another mechanism of dealing with toxic

metals may involve polyphosphates, long chains of ortho-

phosphates, which may sequester metals [27].

Perrin et al. recently reported that Ni exposure promoted

biofilm formation in Escherichia coli cultures, which may

serve as a protective tolerance mechanism. Ni appeared to

be involved in adherence by inducing transcription of

genes encoding curli, the adhesive structures necessary

for biofilm formation [28].

The protective quality of EPS or these other mechanisms

provided by root-associated bacteria suggests that enrich-

ing for certain bacteria may replace the technique of

amending plant root zones with synthetic cross-linked

polyacrylates and hydrogels to protect roots from heavy

metal toxicity [29].

Metal tolerance and resistance: the plant sideIn plants, metal accumulation in the cells may be

regulated by glutathione–phytochelatin-mediated resist-

ance. In this system, glutathione, the same cysteine-

containing tripeptide described above in Rhizobium sp.,

which also has several functions in plant cells including

dealing with toxic oxygen species and amino acid trans-

port, is used to synthesize phytochelatins, which chelate

heavy metals by formation of a thiolate. Thiolates can be

transported to vacuoles for heavy metal storage [30].

Phytochelatins are activated by heavy metals and sca-

venge heavy metals in plant cells [31]. For a review of

plant metal tolerance mechanisms, see [6��].

While some plants deal with moderate levels of toxic

metals by chelation, other plants have the ability to

accumulate extremely high levels of heavy metals and

sequester them in their tissues. Plants that can accumu-


late extremely high concentrations of metals are termed

‘hyperaccumulators’. There have been more than 400

plant species identified as such [5�], including crop

species [32], and the number of hyperaccumulators

among aquatic and wetland plants is rising [33].

Hyperaccumulators may be defined based on biocon-

centration factor (BCF), or the ability to accumulate

metals in plant tissues. For instance, the ability to

accumulate greater than 1000 times the concentration

of Cd (based on concentration of metal in dry weight of

plant) than that in the surrounding medium would be

considered hyperaccumulation [34]. One of the most

studied hyperaccumulators is the terrestrial plant

T. caerulescens, which is a Cd/Zn hyperaccumulator

[35]. Several aquatic plants have been found to

have similar abilities, including Salvinia minima [36],

Potamogeton natans [37], Ceratophyllum demersum [38�],and S. polyrrhiza [39].

Metal hyperaccumulation is an adaptive process between

microbes exposed to heavy metals and plants, requiring

continuous interactions among the co-occurring organ-

isms. A recent proteomics study by Farinati et al. [40��]indicated that the presence of a rhizosphere microbial

population, adapted to heavy-metal-polluted sites,

greatly enhanced the accumulation of metals in shoots

of the hyperaccumulator Arabidopsis halleri.

Aquatic environments include not only macrophytes, but

also algae that may interact with microbes to remove

contaminants from the environment. Algae can be pro-

duced in artificial systems and used to remove contami-

nants. Loutseti et al. used a dried mixture of microalgae

and bacteria to remove Cu and Cd from wastewater [41�].Munoz et al. successfully examined the combination of

the bacterium Ralstonia basilensis and the microalga Chlor-ella sorokiniana on adsorption of Cd, Cu, Ni, and Zn [42].

Moreover, mycorrhizal fungi associated with plants can

enhance uptake of metals when essential metal concen-

trations are low and, vice versa, when metal quantities are

too high mycorrhizae can be effective in alleviating metal

toxicity decreasing plant uptake [43].

Mechanisms for how aquatic plant–microbeinteractions affect phytoremediationprocessesWhile many plants and bacteria have their own mechan-

isms for dealing with heavy metal contaminants, the

interaction of plants and microorganisms may increase

or decrease heavy metal accumulation in plants, depend-

ing on the nature of the plant–microbe interaction.

Because phytoremediation is a relatively new technology,

understanding mechanisms of plant–microbe interactions

in removing contaminants from the environment is

still not well characterized. There have, however, been


Biotech potential of plant–microbe interaction Stout and Nusslein 341

Figure 1

Mechanisms of aquatic plant–microbe associations that support metal phytoremediation.

several ideas about the nature of plant–microbe inter-

actions in metal accumulation (Figure 1).

In their paper describing bacterial enhancement of

Se and Hg uptake by wetland plants, De Souza et al.proposed several possible mechanisms, including

bacterial stimulation of plant metal uptake compounds

such as siderophores; bacterial root growth promotion

increasing the root surface area; bacterial transformation

of elements into more soluble forms; or bacterial stimu-

lation of plant transporters that may transport essential

elements as well as heavy metals (in the case of selenate,

the sulfate transporter) [44�]. Van der Lelie related the

basis of this plant–microbe interaction to bacterial metal

resistance, since the bioavailability of metals could be

altered by bacterial expression of resistance systems

[25��].

Plant growth promotion

One idea is that bacteria promote plant growth, thus

increasing surface area of the plant and allowing more

metal uptake. Certain compounds produced by bacteria

have been shown to promote plant growth, including

siderophores. Siderophores, Fe-chelating compounds,

have been shown to promote plant growth even in the


presence of heavy metals [45,46]. Bacterial production of

siderophores may protect plants from heavy metal

toxicity, increasing plant growth by providing the plants

with sufficient iron and allowing them to overcome the

toxic effects of heavy metals.

Another plant growth promoting compound that has been

studied in relation to heavy metals is 1-aminocyclopro-

pane-1-carboxylic acid deaminase (ACC deaminase).

ACC is an intermediate of ethylene produced by plants

under stress, and bacteria that produce ACC deaminase

can lower the levels of ethylene in plants, promoting plant

growth [47]. Belimov et al. found that bacteria containing

ACC deaminase improve plant growth in metal-polluted

conditions [48].

Bacteria as well as plants can produce the auxin indole-3-

acetic acid (IAA). Rajkumar and Freitas [49] suggested

that IAA indirectly promotes metal accumulation in

plants by increasing plant biomass. Grandlic et al. found

that 76% of plant growth promoting isolates from plants

grown in mine tailings were able to produce IAA when

supplemented with tryptophan, and these bacteria could

promote growth of plants growing in mine tailings for

phytostabilization [50].



Bacterial metal resistance/chelation/EPS

Metal resistance has been described as a necessity for

plant-associated bacteria in contaminated environments

[51]. Van der Lelie related plant metal uptake to bacterial

metal resistance, since the bioavailability of metals could

be altered by expression of bacterial metal resistance

systems [25��]. Faisal and Hasnain inoculated sunflower

plants with Cr resistant bacteria, and found that plant

growth in Cr was improved by inoculation, although

inoculated plants accumulated less Cr than uninoculated

plants [52]. Kunito et al. examined rhizosphere bacteria

from Phragmites grown in Cu. They found EPS production

was greater for rhizosphere bacteria compared to non-

rhizosphere bacteria. Because of Cu binding to bacterial

EPS, rhizosphere soil may become less toxic to bacteria

and also to plants [53].

Alteration of rhizosphere pH

Another possibility could be the lowering of pH in the

rhizosphere by bacteria, which would make metals more

soluble. The rhizosphere pH could be lowered by pro-

cesses listed above, or other mechanisms, such as bac-

terial metal resistance systems. Bravin et al. pointed out

that rhizosphere pH can also be raised by biological

activity; in extremely low pH environments, roots alka-

lized the rhizosphere, making Cu less bioavailable [54].

Abou-Shanab et al. hypothesized that rhizosphere bacteria

of Alyssum murale lowered rhizosphere pH, solubilizing

metal for hyperaccumulation of Ni by the plant [55].

Phytoprotection

As illustrated above, two possibilities may exist for plant–microbe interactions in relation to metals. Bacterial mech-

anisms could lead to increased accumulation of metals in

plants, or bacteria may keep metals from being accumu-

lated by plants at high concentrations that are toxic to the

plant. This may be the case for chelation or EPS pro-

duction by bacteria [52]. Salt suggested that rhizobacteria

promote precipitation of Cd at the root surface, causing

plants to take up less metal [51].

While the studies of plant–microbe interactions in the

rhizosphere have been carried out in mainly terrestrial

systems (although some wetland plants have been used),

these principles could also apply to aquatic systems,

where bacteria are still closely associated with plant roots.

Transgenic plantsThe biotechnological potential of plant–microbe relation-

ships for use in phytoremediation has included research

on transgenic plants. Much of this research has focused on

terrestrial plants, and many engineered plant systems for

phytoremediation have been used to degrade organic

contaminants. However, several recent studies have

focused on transgenic plants and metals. Parkash Dhan-

kher et al. found that tobacco plants expressing the

bacterial arsenate reductase gene, arsC, were more toler-


ant to and accumulated more Cd [56]. Che et al. engin-

eered transgenic cottonwood trees (Populus deltoides) to

express bacterial merB genes, and found that plants were

more resistant to organic Hg compounds than wild-type

plants [57]. Hussein et al. engineered transgenic tobacco

plants through the chloroplast genome with both merAand merB genes, and saw fewer toxic effects of Hg and

more Hg accumulation than in wild-type plants [58].

Plant–microbe symbioses also have been exploited in

transgenics. Wu et al. manufactured a synthetic phyto-

chelatin analog that was expressed in Pseudomonas putidato increase Cd binding, and this engineered bacterium

was then added to sunflower roots to increase Cd accumu-

lation and lessen Cd toxicity in plants [59�]. While few

studies so far have focused on engineering aquatic plants

for decreased metal toxicity and increased metal removal,

a recent study by Moontongchoon et al. focused on water

spinach (Ipomoea aquatica). Expression of genes from

sulfate assimilation pathways in these transgenes pro-

vided elevated Cd tolerance, and could be useful for

remediation of metals in high sulfate environments [60].

Future directionsIn the coming years, projects involving aquatic plant–microbe interactions for the removal of heavy metal

contaminants may become increasingly viable options,

especially in shallow wetland and estuary environments.

Use of constructed wetlands for filtration and remediation

of water is currently a popular method, and understanding

the nature of plant–microbe interactions may improve

this process. Developing new methods to support

microbial activity to either enhance (for phytoextraction)

or reduce (for phytostabilization) the bioavailability of

metal contaminants in the rhizosphere could significantly

improve the efficiency of these remediation techniques.

Plants that hyperaccumulate metals have tremendous

potential for application in remediation of metals in

the environment. Significant progress in phytoremedia-

tion has been made with metals and radionuclides. This

process involves raising plants hydroponically and trans-

planting them into metal-polluted waters where they

absorb and concentrate metals in their roots and shoots,

and can be harvested for disposal. Root exudates lead to

selective recruitment and accumulation of a diverse range

of bacterial species associated with plants.

Besides heavy metals, organic contaminants can also be

removed by aquatic plants and their associated microbial

communities. Unlike metals, which cannot be degraded

and tend to be accumulated by plants, there is evidence

that many organic contaminants are degraded in the

rhizosphere by plant-associated bacteria and are trans-

formed there rather than inside the plant. For instance,

the duckweed S. polyrrhiza and its associated bacteria may

degrade the aromatic compounds phenol, aniline, and 2,4-

dichlorophenol [61], and the reed Phragmites australis and



its associated rhizosphere bacteria might degrade bisphe-

nol [62�]. The marine eelgrass Zostera marina and its

associated bacteria may degrade PAHs and PCBs [63].

Applications have recently been extended to commercial

phytomining, the recovery of precious metals such as

gold, silver, platinum, and palladium in mining [64��].The attractiveness of phytomining should increase if

combined with other technologies such as biofuel pro-

duction. Results reported in the literature indicate that

plant–microbial associations can significantly increase

metal uptake and accumulation.

Many possibilities exist for the large-scale application of

bacterial–plant systems for removal of metals from

aquatic environments. Large, shallow areas with low

levels of contamination are ideal sites for these tech-

niques, and use of transgenic plants and microbes may

allow plants not only to survive, but also to accumulate

metals in areas with higher levels of contaminants.

ConclusionsAquatic phytoremediation of metals, the use of plants to

extract, contain and immobilize, or remove hazardous

substances from aqueous environments is a very promis-

ing area, and several highly efficient examples have

shown the applicability of this process to clean industrial

waste streams, to concentrate heavy metals, and to pre-

serve drinking water and aquatic biodiversity.

Limitations to this technology do exist and must also be

considered. The application of rhizofiltration is limited by

metal availability, concentration, and phytotoxicity.

Environmental factors like light, salinity, temperature,

pH, and presence of multiple heavy metals may affect

metal uptake. Further limitations of phytoremediation

technology are seasonal growth of aquatic plants and

contaminated biomass disposal issues.

Phytoremediation focused on dissolved metals can be

based on the application of both dead or live plant

material or on the cultivation of aquatic plants. Not only

aquatic macrophytes, but also algae and fungi, represent a

cost-effective and eco-friendly technology for environ-

mental cleanup, a green solution often preferred in

political decision-making.

Rhizosphere microbes can reduce metal toxicity and

enhance plant tolerance to dissolved metals, and can

therefore be applied to supply increased phytoprotection

from harmful effects of the metals on plants. In a direct

extension of this idea the bacterial genes coding for metal

resistance can be transplanted into the plant genome to

confer elevated metal tolerance to plants.

Further research in aquatic phytoremediation is needed

to advance understanding of microbe–plant interactions.


Such knowledge would increase the number of poten-

tially widespread applications and their impact such as

the treatment of heavy metals from industrial effluents in

natural and constructed wetlands, or a wastewater metal

stripping phase using rhizofiltration.

A directed functional analysis should investigate plant–microbe interactions at full biological hierarchy, starting

with the genomic, transcriptomic, and proteomic analysis

of plant-associated bacteria [40��] and their extracellular

enzyme activities, all the way to biochemical processes

and cycling that are active within the bacterially influ-

enced rhizosphere. With this understanding the plant–microbe system could be implemented at field-scale,

using naturally adapted indigenous microbes that have

been cultured and enriched in the laboratory. Such a

multidisciplinary and integrated approach may gain

aquatic metal phytoremediation the commercial signifi-

cance in environmental biotechnology it deserves.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

1. Christensen PB, Revsbech NP, Sand-Jensen K: Microsensoranalysis of oxygen in the rhizosphere of the aquaticmacrophyte Littorella uniflora (L.) Ascherson. Plant Physiol1994, 105:847-852.

2.�

Kraemer U: Phytoremediation: novel approaches tocleaning up polluted soils. Curr Opin Biotechnol 2005,16:1-9.

Interesting recent review discussing phytoextraction and transgenicplants, and modern genetic approaches to phytoremediation.

3.��

Rai PK: Heavy metal phytoremediation from aquaticecosystems with special reference to aquatic macrophytes.Crit Rev Env Sci Technol 2009, 39:697-753.

Detailed review of phytoremediation focusing on heavy metals andaquatic plants. Highlights advantages of phytoremediation for use inaquatic systems over conventional technologies and several hypothesesas to why plants hyperaccumulate metals.

4. Flathman PE, Lanza GR: Phytoremediation: currentviews on an emerging green technology. J Soil Contam 1998,7:415-432.

5.�

Prasad MNV, Freitas HMD: Metal hyperaccumulation inplants — biodiversity prospecting for phytoremediationtechnology. Electron J Biotechnol 2003, 6:285-321.

Review of phytoremediation technologies that includes list of knownbacteria, algae, lichens, fungi, and plants that show resistance to metalsand have potential applications for metal removal from the environment.

6.��

Jabeen R, Ahmad A, Iqbal M: Phytoremediation of heavy metals:physiological and molecular mechanisms. Bot Rev 2009,75:339-364.

Detailed review on phytoremediation and mechanisms used by plants toaccumulate and tolerate heavy metals including bioavailability, translo-cation, exclusion, compartmentalization, plant metallothioneins, andphytochelatins, and discussion of how to improve phytoremediationthrough transgenic plants and addition of chelators.

7.��

Murakami M, Nakagawa F, Ae N, Ito M, Arao T: Phytoextractionby rice capable of accumulating Cd at high levels: reduction ofCd content of rice grain. Environ Sci Technol 2009,43:5878-5883.

This paper shows that rice plants, adapted to aquatic/wetland environ-ments, outperform the terrestrial hyperaccumulator Thlaspi caerulescens,which is not well-adapted to this environment, in metal accumulation.



8. Lee M, Yang M: Rhizofiltration using sunflower (Helianthusannuus L.) and bean (Phaseolus vulgaris L. var. vulgaris) toremediate uranium contaminated groundwater. J Hazard Mater2010, 173:589-596.

9. Agunbiade FO, Olu-Owolabi BI, Adebowale KO:Phytoremediation potential of Eichornia crassipes inmetal-contaminated coastal water. Bioresour Technol 2009,100:4521-4526.

10.�

Mishra VK, Tripathi BD: Accumulation of chromium and zincfrom aqueous solutions using water hyacinth (Eichhorniacrassipes). J Hazard Mater 2009, 164:1059-1063.

This article shows that water hyacinth, Eichhornia crassipes, is veryeffective at removing chromium and zinc from aquatic systems.

11.�

Ghassemzadeh F, Yousefzadeh H, Arbab-Zavar MH: Removingarsenic and antimony by Phragmites australis: rhizofiltrationtechnology. J Appl Sci 2008, 8:1668-1675.

This paper shows the potential for arsenic and antimony removal by theaquatic invasive reed Phragmites australis, suggesting that these nui-sance plants may have phytoremediation potential.

12. Rahman MA, Hasegawa H, Ueda K, Maki T, Okumura C,Rahman MM: Arsenic accumulation in duckweed (Spirodelapolyrhiza L.): a good option for phytoremediation.Chemosphere 2007, 69:493-499.

13.�

Hou W, Chen X, Song G, Wang Q, Chi Chang C: Effects of copperand cadmium on heavy metal polluted waterbody restorationby duckweed (Lemna minor). Plant Physiol Biochem 2007,45:62-69.

Points out that duckweed (Lemna minor) would be a suitable candidatefor phytoremediation but also studies mechanisms of toxic effects ofcadmium and copper on the plants.

14. Uysal Y, Taner F: Effect of pH, temperature, and leadconcentration on the bioremoval of lead from water usingLemna minor. Int J Phytoremed 2009, 11:591-608.

15. Khellaf N, Zerdaoui M: Phytoaccumulation of zinc by the aquaticplant, Lemna gibba L.. Bioresour Technol 2009, 100:6137-6140.

16. Megateli S, Semsari S, Couderchet M: Toxicity and removal ofheavy metals (cadmium, copper, and zinc) by Lemna gibba.Ecotoxicol Environ Saf 2009, 72:1774-1780.

17.�

Rai PK, Tripathi BD: Comparative assessment of Azolla pinnataand Vallisneria spiralis in Hg removal from G.B. Pant Sagar ofSingrauli industrial region, India. Environ Monit Assess 2009,148:75-84.

This work compares the mercury removal abilities of two aquatic plants;Azolla, a free-floating fern, and Vallisneria, a submerged macrophyte.While both were able to accumulate mercury, Azolla was able to removemore than Vallisneria.

18. Abhilash PC, Pandey VC, Srivastava P, Rakesh PS, Chandran S,Singh N, Thomas AP: Phytofiltration of cadmium from water byLimnocharis flava (L.) Buchenau grown in free-floating culturesystem. J Hazard Mater 2009, 170:791-797.

19. Coombs JM, Barkay T: New findings on evolution of metalhomeostasis genes: evidence from comparative genomeanalysis of bacteria and archaea. Appl Environ Microbiol 2005,71:7083-7091.

20. Gadd GM: Metals and microorganisms: a problem ofdefinition. FEMS Microbiol Lett 1992, 79:197-203.

21. Nies DH: Efflux-mediated heavy metal resistance inprokaryotes. FEMS Microbiol Rev 2003, 781:1-27.

22. Huckle JW, Morby AP, Turner JS, Robinson NJ: Isolation of aprokaryotic metallothionein locus and analysis oftranscriptional control by trace metal ions. Mol Microbiol 1993,7:177-187.

23. Ybarra GR, Webb R: Effects of divalent metal cations andresistance mechanisms of the cyanobacteriumSynechococcus sp. strain PCC 7942. J Hazard Subst Res 1999,2:1-9.

24. Pages D, Rose J, Conrod S, Cuine S, Carrier P, Heulin T,Achouak W: Heavy metal tolerance in Stenotrophomonasmaltophilia. PLoS One 2008, 3:e1539.


25.��

Van der Lelie D, Corbisier P, Diels L, Gills A, Lodewyckx C,Mergeay M, Taghavi S, Spelmans N, Vangronsveld J: The role ofbacteria in the phytoremediation of heavy metals. InPhytoremediation of Contaminated Soil and Water. Edited by TerryN, Banuelos GS. Lewis Publishers; 2000:265-281.

This book chapter outlines some potential ideas about the nature ofplant–microbe interactions in phytoremediation.

26. Figueira EM, Lima AI, Pereira SI: Cadmium tolerance plasticity inRhizobium leguminosarum bv. viciae: glutathione as adetoxifying agent. Can J Microbiol 2005, 51:7-14.

27. Alvarez S, Jerez CA: Copper ions stimulate polyphosphatedegradation and phosphate efflux in Acidithiobacillusferrooxidans. Appl Environ Microbiol 2004, 70:5177-5182.

28. Perrin C, Briandet R, Jubelin G, Lejeune P, Mandrand-Berthelot MA, Rodrigue A, Dorel C: Nickel promotes biofilmformation by Escherichia coli K-12 strains that produce curli.Appl Environ Microbiol 2009, 75:1723-1733.

29. Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C,Kapulnik Y, Ensley BD, Raskin I: Enhanced accumulation of Pb inindian mustard by soil-applied chelating agents. Environ SciTechnol 1997, 31:860-865.

30. Mendoza-Cozatl DG, Moreno-Sanchez R: Control of glutathioneand phytochelatin synthesis under cadmium stress. Pathwaymodeling for plants. J Theor Biol 2006, 238:919-936.

31. Blum R, Beck A, Korte A, Stengel A, Letzel T, Lendzian K, Grill E:Function of phytochelatin synthase in catabolism ofglutathione-conjugates. Plant J 2007, 49:740-749.

32. Vamerali T, Bandiera M, Mosca G: Field crops forphytoremediation of metal-contaminated land. A review.Environ Chem Lett 2010, 8:1-17.

33. Prasad MNV, Malec P, Waloszek A, Bojko M, Strzalka K:Physiological responses of Lemna triscula L. (duckweed) tocadmium and copper bioaccumulation. Plant Sci 2001,161:881-889.

34. Zayed A, Gowthaman S, Terry N: Phytoaccumulation of traceelements by wetland plants: I. Duckweed. J Environ Qual 1998,27:715-721.

35. Mijovilovich A, Leitenmaier B, Meyer-Klaucke W, Kroneck PM,Gotz B, Kupper H: Complexation and toxicity of copper inhigher plants. II. Different mechanisms for copper versuscadmium detoxification in the copper-sensitive cadmium/zinchyperaccumulator Thlaspi caerulescens (Ganges Ecotype).Plant Physiol 2009, 151:715-731.

36. Sanchez-Galvan G, Monroy O, Gomez J, Olguin EJ: Assessmentof the hyperaccumulating lead capacity of Salvinia minimausing bioadsorption and intracellular accumulation factors.Water Air Soil Pollut 2008, 194:77-90.

37. Fritioff A, Greger M: Uptake and distribution of Zn, Cu, Cd, andPb in an aquatic plant, Potamogeton natans. Chemosphere2006, 63:220-227.

38.�

Robinson B, Kim N, Marchetti M, Moni C, Schroeter L, van denDijssel C, Milne G, Clothier B: Arsenic hyperaccumulation byaquatic macrophytes in the Taupo Volcanic Zone, NewZealand. Environ Exp Bot 2006, 58:206-215.

This work examines arsenic accumulation in aquatic and terrestrial plantsat the Taupo Volcanic Zone. Aquatic plants accumulated high levels ofarsenic, most of which appeared to be bound to iron plaques at roots.

39. John R, Ahmad P, Gadgil K, Sharma S: Effect of cadmium andlead on growth, biochemical parameters and uptake in Lemnapolyrrhiza L.. Plant Soil Environ 2008, 54:262-270.

40.��

Farinati S, DalCorso G, Bona E, Corbella M, Lampis S, Cecconi D,Polati R, Berta G, Vallini G, Furini A: Proteomic analysis ofArabidopsis halleri shoots in response to the heavy metalscadmium and zinc and rhizosphere microorganisms.Proteomics 2009, 9:4837-4850.

This recent proteomic analysis emphasized the role of plant–microbeinteraction in metal hyperaccumulation. The proteome of shoots of thehyperaccumulator Arabidopsis halleri was analyzed for the effect of plant–microbe interaction on the accumulation efficiency. While it is wellaccepted now that plant metal uptake is strongly influenced by rhizo-sphere microbes, these findings suggest for the first time that metal



hyperaccumulation is an adaptive process requiring continuous interac-tions among co-occurring organisms.

41.�

Loutseti S, Danielidis DB, Economou-Amilli A, Katsaros C,Santas R, Santas P: The application of a micro-algal/bacterialbiofilter for the detoxification of copper and cadmium metalwastes. Bioresour Technol 2009, 100:2099-2105.

This study is a good example how microbial biomass of dried microalgaeand bacteria can be applied to abiotically detoxify aqueous metal waste-waters by sorption. Subsequent acidic desorption reached 100% effi-ciency.

42. Munoz R, Alvarez MT, Munoz A, Terrazas E, Guieysse B,Mattiasson B: Sequential removal of heavy metals ions andorganic pollutants using an algal–bacterial consortium.Chemosphere 2006, 63:903-911.

43. Frey B, Zierold K, Brunner I: Extracellular complexation of Cd inthe Hartig net and cytosolic Zn sequestration in the fungalmantle of Picea abies–Hebeloma crustuliniformeectomycorrhizas. Plant Cell Environ 2000, 23:1257-1265.

44.�

De Souza MP, Huang CPA, Chee N, Terry N: Rhizospherebacteria enhance the accumulation of selenium and mercuryin wetland plants. Planta 1999, 209:259-263.

One of the first studies that demonstrated the role of rhizosphere bacteriain facilitating increased heavy metal accumulation in wetland plants.

45. Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R: Isolationand functional characterization of siderophore-producinglead- and cadmium-resistant Pseudomonas putida KNP9. CurrMicrobiol 2005, 50:233-237.

46. Burd GI, Dixon DG, Glick BR: Plant growth-promoting bacteriathat decrease heavy metal toxicity in plants. Can J Microbiol2000, 46:237-245.

47. Dell’Amico E, Cavalca L, Andreoni V: Analysis of rhizobacterialcommunities in perennial Graminaceae from polluted watermeadow soil, and screening of metal-resistant, potentiallyplant growth-promoting bacteria. FEMS Microbiol Ecol 2005,52:153-162.

48. Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN,Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C,Preisfeld A et al.: Characterization of plant growth promotingrhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol2001, 47:642-652.

49. Rajkumar M, Freitas H: Effects of inoculation of plant-growthpromoting bacteria on Ni uptake by Indian mustard. BioresourTechnol 2008, 99:3491-3498.

50. Grandlic CJ, Mendez MO, Chorover J, Machado B, Maier RM:Plant growth-promoting bacteria for phytostabilization ofmine tailings. Environ Sci Technol 2008, 42:2079-2084.

51. Salt DE, Benhamou N, Leszczyniecka M, Raskin I: A possible rolefor rhizobacteria in water treatment by plant roots. Int JPhytoremed 1999, 1:67-79.

52. Faisal M, Hasnain S: Chromate resistant Bacillus cereusaugments sunflower growth by reducing toxicity of Cr(VI). JPlant Biol 2005, 48:187-194.

53. Kunito T, Saeki K, Nagaoka K, Oyaizu H, Matsumoto S:Characterization of copper-resistant bacterial community inrhizosphere of highly copper-contaminated soil. Eur J Soil Biol2001, 37:95-102.


54. Bravin MN, Tentscher P, Rose J, Hinsinger P: Rhizosphere pHgradient controls copper availability in a strongly acidic soil.Environ Sci Technol 2009, 43:5686-5691.

55. Abou-Shanab RA, Delorme TA, Angle JS, Chaney RL, Ghanem K,Moawad H, Ghozlan HA: Phenotypic characterization ofmicrobes in the rhizosphere of Alyssum murale. Int JPhytoremed 2003, 5:367-379.

56. Dhankher OP, Shasti NA, Rosen BP, Fuhrmann M, Meagher RB:Increased cadmium tolerance and accumulation by plantsexpressing bacterial arsenate reductase. New Phytol 2003,159:431-441.

57. Che D, Meagher RB, Heaton ACP, Lima A, Rugh CL, Merkle SA:Expression of mercuric ion reductase in Eastern cottonwood(Populus deltoides) confers mercuric ion resistance. PlantBiotechnol J 2003, 1:311-319.

58. Hussein HS, Ruiz ON, Terry N, Daniell H: Phytoremediation ofmercury and organomercurials in chloroplast transgenicplants: enhanced root uptake, translocation to shoots, andvolatilization. Environ Sci Technol 2007, 41:8439-8446.

59.�

Wu CH, Wood TK, Mulchandani A, Chen W: Engineering plant–microbe symbiosis for rhizoremediation of heavy metals. ApplEnviron Microbiol 2006, 72:1129-1134.

The idea for an effective cleanup technology is demonstrated by combin-ing expression of a metal-binding peptide in a rhizobacterium with sun-flower roots. Both organisms had significantly improved growthcharacteristics and cadmium tolerance, and the plant had 40% highermetal uptake.

60. Moontongchoon P, Chadchawan S, Leepipatpiboon N,Akaracharanya A, Shinmyo A, Sano H: Cadmium-tolerance oftransgenic Ipomoea aquatica expressing serineacetyltransferase and cysteine synthase. Plant Biotechnol2008, 25:201-203.

61. Toyama T, Yu N, Kumada H, Sei K, Ike M, Fujita M: Acceleratedaromatic compounds degradation in aquatic environment byuse of interaction between Spirodela polyrrhiza and bacteria inits rhizosphere. J Biosci Bioeng 2006, 101:346-353.

62.�

Toyama T, Sato Y, Inoue D, Sei K, Chang YC, Kikuchi S, Ike M:Biodegradation of bisphenol A and bisphenol F in therhizosphere sediment of Phragmites australis. J Biosci Bioeng2009, 108:147-150.

This recent study of plant–microbe interactions in phytoremediation couldsuccessfully show that interactions between an aquatic macrophyte (P.australis) and specific root-associated bacteria accelerate the removal ofbisphenols from sediment. Here the rhizosphere bacteria involved havebeen studied. This finding goes beyond previous studies by this groupwhere mere rhizosphere oxidation, the ability of plants to release oxygeninto the rhizosphere, was thought to be the driver for the biodegradationof organic compounds.

63. Huesemann MH, Hausmann TS, Fortman TJ, Thom RM,Cullinan V: In situ phytoremediation of PAH- and PCB-contaminated marine sediments with eelgrass (Zosteramarina). Ecol Eng 2009, 35:1395-1404.

64.��

Sheoran V, Sheoran AS, Poonia P: Phytomining: a review. MinerEng 2009, 22:1007-1019.

An excellent recent review of various aspects of phytomining along withthe advantages, limitations, and future feasibility to employ plants(macrophytes and microcosms) to bioharvest desired metals from ter-restrial environments, particularly those associated with sub-economicpotential. Examples discussed in detail are Ni, Co, Ti, Au, and Ag.


Biotechnological Potential Aquatic Plant Microbe Interactions COB2010

Documents

Transcript of Biotechnological Potential Aquatic Plant Microbe Interactions COB2010