Analysis of Microbial Diversity in Soil under Ginger Cultivation...microbe and microbe-ginger...

Research ArticleAnalysis of Microbial Diversity in Soil underGinger Cultivation

Yiqing Liu1 LinWu1 XingwenWu2 Honghai Li3 Qinhong Liao1

Xiaojing Zhang4 Zhiqiang Sun4 andWenhua Li4

1Chongqing Key Laboratory of Economic Plant Biotechnology Collaborative Innovation Center ofSpecial Plant Industry in Chongqing Institute of Special Plants College of Forestry amp Life ScienceChongqing University of Arts and Sciences Yongchuan Chongqing 402160 China2Liangping Agro-Technical Extension Station Liangping Chongqing 405200 China3Chongqing Engineering and Technology Research Center for Utilization of Ginger ResourceChongqing Tianpei Agro-Tech Co Ltd Yongchuan Chongqing 402189 China4Yantai Lvyun Biotechnology Co Ltd Yantai 264003 China

Correspondence should be addressed to Honghai Li 1207118074qqcom

Received 22 May 2017 Accepted 11 September 2017 Published 23 October 2017

Academic Editor Maurizio Sanguinetti

Copyright copy 2017 Yiqing Liu et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Ginger is a perennialmonocotyledonous herbwhich can be used as both a vegetable and amedicinal plantHowever it is susceptibleto various plant pathogens Microbial diversity in soil is related closely to the health and productivity of plant crops includingginger In the current study we compared microbial diversity from soil samples under ginger cultivation (disease incidence ofgt50 [relatively unhealthy sample] versus disease incidence of lt10 [relatively healthy sample]) The bacterial and fungal taxawere analyzed by Illumina-based sequencing with 16S and ITS identification respectively Both bacterial and fungal OTUs weresignificantly more in the healthy soil sample than the unhealthy sample Moreover the dominant bacterial and fungal genera weredetected to be different in each sample Rhodanobacter and Kaistobacter were the dominant bacterial genera in the healthy samplewhile Rhodoplanes and Bradyrhizobium were the dominant genera in the unhealthy sample For fungal analysis CladosporiumCryptococcus and Tetracladium were the dominant genera in the healthy sample while Lecanicillium Pochonia and Rhodotorulawere the dominant genera in the unhealthy sample Collectively the basic information of microbial diversity in ginger soil ishelpful for elucidating the ginger-microbe interactions and potentially selecting suitable plant growth-promoting rhizobacteriaand biocontrol agents for ginger production

1 Introduction

Ginger (Zingiber officinale) is a perennial monocotyledonousherb which can be used as both a vegetable and a medic-inal plant It is widely employed in Chinese Ayurvedicmedicines and home remedies since antiquity for manyailments including pain inflammation and gastrointestinaldisorders [1] However ginger is subject to various diseasesduring growth stages [2ndash5] The occurrence of these diseasesresults in significant yield reductions in ginger For instanceEnterobacter cloacae causes ginger rhizome rot [6] whileErwinia chrysanthemi is the causal agent of ginger soft rot [7]Root-rot disease caused by the fungal pathogen Pythium

myriotylum was reported to decimate ginger in field plant-ings when temperatures ranged from 26 to 30∘C and thesoil was saturated with water due to continuous rainfall [8]Ginger rhizomes infected with Fusarium oxysporum exhibityellow shoots and die after a few weeks [9] and it is also adevastating postharvest disease for stored ginger [10]

Soil microbial community plays an important role innutrient mobilisation and uptake for plant They promoteplant growth and suppress disease by their various activitieslike phosphate and sulphate solubilisation plant growthpromotion siderophore production nitrogen fixation den-itrification immune modulation signal transduction andpathogen control [11]Theobjectives of the present studywere

HindawiScientificaVolume 2017 Article ID 8256865 4 pageshttpsdoiorg10115520178256865

2 Scientifica

to analyze and compare the microbial diversity from the soilunder the cultivation of ginger with low disease incidence(healthy sample) and high disease incidence (unhealthysample) Specially total microbial DNAof ginger soil sampleswas purified and analyzed by Illumina-based sequencingThebacterial and fungal communities were further comparedand the vertically transmitted bacterial and fungal taxa wereelucidated in the study

2 Material and Methods

21 Soil Sampling and DNA Extraction The soil sampleswere collected from the organic ginger field in YongchuanChongqing China (N29∘101015840578010158401015840 E105∘50101584017710158401015840) in Sep2016This organic farmwith total of 50000m2 area is dividedinto 100 planting units with each of 500m2 area Whenthe gingers were harvested in Sep 2016 it was found thatthe disease incidence varied among each planting unit Inorder to analyze the microbial diversity the rhizosphericsoil samples were collected from two groups (healthy groupversus disease group) Soil samples were collected at a depthof approximately 15 cm in sterile polythene bags and storedin refrigerator until DNA extraction In Group I the soilsamples were taken from nine ginger-planting units in whichthe disease incidencewas lower than 10 inGroup II the soilsamples were taken from nine ginger-planting units in whichthe disease incidence was more than 50

The soil samples from the two groups above were usedfor total DNA extractionThe total DNA was extracted usingEZNA Soil DNA Kit (Omega Bio-Tek USA) according tothe manufacturersquos instruction Briefly about 1 g soil samplewas added to 15mL centrifuge tube with glass beads TotalDNA was obtained after the procedures of lysis centrifuga-tion binding on DNA binding column elution and purifica-tion Total DNA concentration and purity weremonitored on1 agarose gels

22 Amplicon Generation and Illumina MiSeq Sequenc-ing The pair of primers 515F (51015840-GTGCCAGCMGCC-GCGGTAA-31015840) and 907R (51015840-CCGTCAATTCCTTTG-AGTTT-31015840) were used to amplify the V4-V5 regions ahypervariable area of the 16S rRNA gene The primersITS5-1737F (51015840-GGAAGTAAAAGTCGTAACAAGG-31015840) andITS2-2043R (51015840-GCTGCGTTCTTCATCGATGC-31015840) target-ing the ITS1 regions of fungal rRNA genes were adopted toanalyze fungal taxa [12] Both forward and reverse primerswere tagged with adapter pad and linker sequencing Eachbarcode sequencewas added to the reverse primer for poolingmultiple samples into one run of sequencing All PCR ampli-fications were performed in terms of previously reportedmethod [13] The reaction conditions were as follows aninitial denaturation at 98∘C for 1min each of 30 cycles at 98∘Cfor 10 s 55∘C for 30 s and 72∘C for 60 s with a final extensionat 72∘C for 5min After mixing the PCR products of thetriplicate detectionwas implemented by 2 (wv) agarose gelelectrophoresis and then the PCR products were purified bythe AxyPrep Gel Extraction Kit (Axygen USA) Ampliconsfrom each reaction mixture were quantified fluorometricallynormalized and pooled at equimolar ratios based on the

Table 1 Number of OTUs in the samples

Microbial samples OTUsBacteria

Sample 1 1347Sample 2 1179Sample 3 1506Sample 4 1661

FungiSample 1 183Sample 2 196Sample 3 202Sample 4 221

Note Samples 1 and 2 represent the two replicates of soil samples under gingercultivation with disease incidence of gt50 (relatively unhealthy sample)while Samples 3 and 4 represent the two replicates of soil samples underginger cultivation with disease incidence oflt10 (relatively healthy sample)

concentration of each amplicon The sequencing librarieswere generated using NEB Next Ultra DNA Library PrepKit for Illumina (New England Biolabs) following manufac-turerrsquos recommendations and index codes were added Thelibrary quality was assessed on the Qubit 20 Fluorometer(Thermo Scientific) and Agilent Bioanalyzer 2100 system(Agilent Technologies) Finally the libraries were sequencedon an Illumina MiSeq platform [14 15]

23 Data Preprocessing All sequence reads with the sametag were assigned to the same sample according to theunique barcodes (raw tags)The raw tags were further filteredby clean tags and the quality of clean tags was detectedby Qiime (httpqiimeorgindexhtml) [16 17] Rarefactionanalysis was implemented based on MOTHUR packageusing operational taxonomic units (OTUs) grouped at 97sequences similarity [18] The numbers of randomly selectedsequences and corresponding OTUs under the sobs diversityindex were employed as the variables

3 Results and Discussion

The soil provides a great variety of microhabitats for myriadorganisms of different size physiological activity behaviorand ecosystem function [19] The extent of the diversityof microorganisms in soil is critical to the maintenanceof health and quality of soil and plant as a wide rangeof microorganisms is involved in important soil functions[20] Recently there have been a few studies on reports ofginger diseases [14 15 21 22] However to the best of ourknowledge the reports on soil microbes in ginger fields arelimited In the present study we compared the microbialdiversity from soil samples of ginger-planting field (gingerwith low disease incidence [healthy sample] versus gingerwith high disease incidence [unhealthy sample]) The dataof this present study showed that both bacterial and fungalOTUs were significantly more in the healthy soil samplethan the unhealthy sample (Table 1) These findings wereconsistent with the previous study about microbial diversityin the soil under cultivation of potato [23] and maize [24]

Scientifica 3

100

80

60

40

20

01 2 3 4

Relat

ive a

bund

ance

()

AquicellaArthrobacterBacillusBradyrhizobiumBurkholderiaCandidatus_KoribacterCandidatus_SolibacterDA101

GemmataHylemonellaKaistobacter

LactococcusMycobacteriumPlanctomycesPseudomonasRhodanobacterRhodoplanesSalinibacteriumSphingomonasStenotrophomonasUnclassifiedOthers (lt05)

Figure 1 Relative abundance of bacterial genera Samples 1 and2 represent the two replicates of relatively unhealthy soil sampleswhile Samples 3 and 4 represent the two replicates of relativelyhealthy soil samples

More specially the dominant bacterial and fungal generawere detected to be different in each sample Rhodanobacterand Kaistobacter were the dominant bacterial genera in thehealthy sample while Rhodoplanes and Bradyrhizobiumwerethe dominant genera in the unhealthy sample (Figure 1)Rho-danobacter spathiphylli sp Nov was isolated from a gammaproteobacterium isolated from the roots of Spathiphyllumplants and showed biocontrol activity towards the root-rotplant pathogen Cylindrocladium spathiphylli [25] For fungalanalysis Cryptococcus Cladosporium and Tetracladiumwerethe dominant genera in the healthy sample while Lecanicil-lium Pochonia and Rhodotorula were the dominant generain the unhealthy sample (Figure 2) Cryptococcus genus hasbeen reported to be with potential plant growth-promotingtraits [26] and Lecanicillium fungicola is a causal agent of drybubble disease for many crops [27]

4 Conclusions

The current knowledge concerning the microbial diversityparticularly bacteria and fungi in ginger field has thepotential to understand the complex ecosystem of microbe-microbe and microbe-ginger interaction The dominant

Alternaria_alternataCryptococcus_aeriusCryptococcus_terricolaCryptococcus_victoriaeCyberlindnera_jadiniiFusarium_oxysporum_f_sp_melonisGuehomyces_pullulansHerpotrichia_juniperiLeptosphaeria_sp_ntu59Lophiostoma_sp_CBS_109932Microascaceae_sp

Mortierella_polygoniaMortierella_parvispora

Mortierella_sp_04NY02Mycoarthris_corallinaParaphoma_spPochonia_bulbillosaPseudogymnoascus_verrucosusRhodotorula_ferulicaSistotrema_spTetracladium_maxilliformeTremellales_spTricladium_spVerticillium_nigrescensUnclassifiedOthers (lt05)

100

80

60

40

20

01 2 3 4

Relat

ive a

bund

ance

()

Figure 2 Relative abundance of fungal genera Samples 1 and 2represent the two replicates of relatively unhealthy soil sampleswhile Samples 3 and 4 represent the two replicates of relativelyhealthy soil samples

bacterial and fungal genera in the ginger soil samples (healthysample versus unhealthy sample) identified have the potentialto explore biocontrol agents and pathogens This studyprovides implications for maintenance of soil health andsustainable agriculture of ginger production

Conflicts of Interest

The authors declare that they have no conflicts of interest

4 Scientifica

Acknowledgments

This work was supported by the Scientific Research Fundof Chongqing Education Commission (KJZH14216) andChongqing Key Discipline Construction of Forestry

References

[1] K Srinivasan ldquoGinger rhizomes (Zingiber officinale) a spicewith multiple health beneficial potentialsrdquo PharmaNutritionvol 5 no 1 pp 18ndash28 2017

[2] Q Peng Y Yuan and M Gao ldquoBacillus pumilus a novel gingerrhizome rot pathogen in Chinardquo Plant Disease vol 97 no 10pp 1308ndash1315 2013

[3] V Shanmugam H Thakur J Kaur S Gupta S Rajkumarand N P Dohroo ldquoGenetic diversity of Fusarium spp incitingrhizome rot of ginger and itsmanagement by PGPR consortiumin the western Himalayasrdquo Biological Control vol 66 no 1 pp1ndash7 2013

[4] D P Le M Smith G W Hudler and E Aitken ldquoPythiumsoft rot of ginger Detection and identification of the causalpathogens and their controlrdquo Crop Protection vol 65 pp 153ndash167 2014

[5] D Prasath R KarthikaN THabeeba et al ldquoComparison of thetranscriptomes of ginger (Zingiber officinale Rosc) and mangoginger (Curcuma amada Roxb) in response to the bacterial wiltinfectionrdquo PLoS ONE vol 9 no 6 Article ID e99731 2014

[6] S D Jolad R C Lantz J C Guan R B Bates and B NTimmermann ldquoCommercially processed dry ginger (Zingiberofficinale) composition and effects on LPS-stimulated PGE

2

productionrdquo Phytochemistry vol 66 no 13 pp 1614ndash1635 2005[7] A M Stirling ldquoErwinia chrysanthemi the cause of soft rot

in ginger (Zingiber officinale) in Australiardquo Australasian PlantPathology vol 31 no 4 pp 419-420 2002

[8] G R Stirling U Turaganivalu A M Stirling M F Lomavatuand M K Smith ldquoRhizome rot of ginger (Zingiber officinale)caused by Pythium myriotylum in Fiji and Australiardquo Aus-tralasian Plant Pathology vol 38 no 5 pp 453ndash460 2009

[9] KANishijimaAMAlvarez P RHepperly et al ldquoAssociationof Enterobacter cloacae with rhizome rot of edible ginger inHawaiirdquo Plant Disease vol 88 no 12 pp 1318ndash1327 2004

[10] Y Liu M Wisniewski J F Kennedy Y Jiang J Tang andJ Liu ldquoChitosan and oligochitosan enhance ginger (Zingiberofficinale Roscoe) resistance to rhizome rot caused by Fusariumoxysporum in storagerdquoCarbohydrate Polymers vol 151 pp 474ndash479 2016

[11] O Prakash R Sharma P Rahi and N Karthikeyan ldquoRole ofMicroorganisms in Plant Nutrition and Healthrdquo Nutrient UseEfficiency From Basics to Advance pp 125ndash161 2015

[12] P H Degnan and H Ochman ldquoIllumina-based analysis ofmicrobial community diversityrdquo The ISME Journal vol 6 no1 pp 183ndash194 2012

[13] S Jiao Z Liu Y Lin J Yang W Chen and G Wei ldquoBacterialcommunities in oil contaminated soils Biogeography and co-occurrence patternsrdquo Soil Biology amp Biochemistry vol 98 pp64ndash73 2016

[14] B Huang J Li W Fang et al ldquoEffect of Soil Fumigation onDegradation of Pendimethalin and Oxyfluorfen in Laboratoryand Ginger Field Studiesrdquo Journal of Agricultural and FoodChemistry vol 64 no 46 pp 8710ndash8721 2016

[15] Y Huang Z KuangWWang and L Cao ldquoExploring potentialbacterial and fungal biocontrol agents transmitted from seedsto sprouts of wheatrdquo Biological Control vol 98 pp 27ndash33 2016

[16] J G Caporaso C L Lauber W A Walters et al ldquoUltra-high-throughputmicrobial community analysis on the IlluminaHiSeq andMiSeq platformsrdquoThe ISME Journal vol 6 no 8 pp1621ndash1624 2012

[17] N A Bokulich S Subramanian J J Faith et al ldquoQuality-filtering vastly improves diversity estimates from Illuminaamplicon sequencingrdquo Nature Methods vol 10 no 1 pp 57ndash592013

[18] R C Edgar ldquoUPARSE highly accurate OTU sequences frommicrobial amplicon readsrdquo Nature Methods vol 10 no 10 pp996ndash998 2013

[19] H Ferris and H Tuomisto ldquoUnearthing the role of biologicaldiversity in soil healthrdquo Soil Biology amp Biochemistry vol 85 pp101ndash109 2015

[20] P Garbeva J A Van Veen and J D Van Elsas ldquoMicrobialdiversity in soil selection of microbial populations by plant andsoil type and implications for disease suppressivenessrdquo AnnualReview of Phytopathology vol 42 pp 243ndash270 2004

[21] G E Thomas K A Geetha L Augustine S Mamiyil andG Thomas ldquoAnalyses between reproductive behavior geneticdiversity and Pythium responsiveness in Zingiber spp revealan adaptive significance for hemiclonalityrdquo Frontiers in PlantScience vol 7 no 2016 article no 1913 2016

[22] X Liu D Yan C Ouyang et al ldquoOils extracted from Eupato-rium adenophorum leaves show potential to control Phythiummyriotylum in commercially-grown gingerrdquo PLoS ONE vol 12no 5 p e0176126 2017

[23] R P Larkin ldquoRelative effects of biological amendments andcrop rotations on soil microbial communities and soilbornediseases of potatordquo Soil Biology amp Biochemistry vol 40 no 6pp 1341ndash1351 2008

[24] P Garbeva J Postma J A Van Veen and J D Van Elsas ldquoEffectof above-ground plant species on soil microbial communitystructure and its impact on suppression of Rhizoctonia solaniAG3rdquo Environmental Microbiology vol 8 no 2 pp 233ndash2462006

[25] D De Clercq S Van Trappen I Cleenwerck et al ldquoRho-danobacter spathiphylli sp nov a gammaproteobacteriumisolated from the roots of Spathiphyllum plants grown ina compost-amended potting mixrdquo International Journal ofSystematic and Evolutionary Microbiology vol 56 no 8 pp1755ndash1759 2006

[26] P Nutaratat N Srisuk P Arunrattiyakorn and S LimtongldquoPlant growth-promoting traits of epiphytic and endophyticyeasts isolated from rice and sugar cane leaves in ThailandrdquoFungal Biology vol 118 no 8 pp 683ndash694 2014

[27] R L Berendsen J J P Baars S I C Kalkhove L G Lugones HA B WoSten and P A H M Bakker ldquoLecanicillium fungicolaCausal agent of dry bubble disease in white-buttonmushroomrdquoMolecular Plant Pathology vol 11 no 5 pp 585ndash595 2010

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2 Scientifica

to analyze and compare the microbial diversity from the soilunder the cultivation of ginger with low disease incidence(healthy sample) and high disease incidence (unhealthysample) Specially total microbial DNAof ginger soil sampleswas purified and analyzed by Illumina-based sequencingThebacterial and fungal communities were further comparedand the vertically transmitted bacterial and fungal taxa wereelucidated in the study

2 Material and Methods

21 Soil Sampling and DNA Extraction The soil sampleswere collected from the organic ginger field in YongchuanChongqing China (N29∘101015840578010158401015840 E105∘50101584017710158401015840) in Sep2016This organic farmwith total of 50000m2 area is dividedinto 100 planting units with each of 500m2 area Whenthe gingers were harvested in Sep 2016 it was found thatthe disease incidence varied among each planting unit Inorder to analyze the microbial diversity the rhizosphericsoil samples were collected from two groups (healthy groupversus disease group) Soil samples were collected at a depthof approximately 15 cm in sterile polythene bags and storedin refrigerator until DNA extraction In Group I the soilsamples were taken from nine ginger-planting units in whichthe disease incidencewas lower than 10 inGroup II the soilsamples were taken from nine ginger-planting units in whichthe disease incidence was more than 50

The soil samples from the two groups above were usedfor total DNA extractionThe total DNA was extracted usingEZNA Soil DNA Kit (Omega Bio-Tek USA) according tothe manufacturersquos instruction Briefly about 1 g soil samplewas added to 15mL centrifuge tube with glass beads TotalDNA was obtained after the procedures of lysis centrifuga-tion binding on DNA binding column elution and purifica-tion Total DNA concentration and purity weremonitored on1 agarose gels

22 Amplicon Generation and Illumina MiSeq Sequenc-ing The pair of primers 515F (51015840-GTGCCAGCMGCC-GCGGTAA-31015840) and 907R (51015840-CCGTCAATTCCTTTG-AGTTT-31015840) were used to amplify the V4-V5 regions ahypervariable area of the 16S rRNA gene The primersITS5-1737F (51015840-GGAAGTAAAAGTCGTAACAAGG-31015840) andITS2-2043R (51015840-GCTGCGTTCTTCATCGATGC-31015840) target-ing the ITS1 regions of fungal rRNA genes were adopted toanalyze fungal taxa [12] Both forward and reverse primerswere tagged with adapter pad and linker sequencing Eachbarcode sequencewas added to the reverse primer for poolingmultiple samples into one run of sequencing All PCR ampli-fications were performed in terms of previously reportedmethod [13] The reaction conditions were as follows aninitial denaturation at 98∘C for 1min each of 30 cycles at 98∘Cfor 10 s 55∘C for 30 s and 72∘C for 60 s with a final extensionat 72∘C for 5min After mixing the PCR products of thetriplicate detectionwas implemented by 2 (wv) agarose gelelectrophoresis and then the PCR products were purified bythe AxyPrep Gel Extraction Kit (Axygen USA) Ampliconsfrom each reaction mixture were quantified fluorometricallynormalized and pooled at equimolar ratios based on the

Table 1 Number of OTUs in the samples

Microbial samples OTUsBacteria

Sample 1 1347Sample 2 1179Sample 3 1506Sample 4 1661

FungiSample 1 183Sample 2 196Sample 3 202Sample 4 221

Note Samples 1 and 2 represent the two replicates of soil samples under gingercultivation with disease incidence of gt50 (relatively unhealthy sample)while Samples 3 and 4 represent the two replicates of soil samples underginger cultivation with disease incidence oflt10 (relatively healthy sample)

concentration of each amplicon The sequencing librarieswere generated using NEB Next Ultra DNA Library PrepKit for Illumina (New England Biolabs) following manufac-turerrsquos recommendations and index codes were added Thelibrary quality was assessed on the Qubit 20 Fluorometer(Thermo Scientific) and Agilent Bioanalyzer 2100 system(Agilent Technologies) Finally the libraries were sequencedon an Illumina MiSeq platform [14 15]

23 Data Preprocessing All sequence reads with the sametag were assigned to the same sample according to theunique barcodes (raw tags)The raw tags were further filteredby clean tags and the quality of clean tags was detectedby Qiime (httpqiimeorgindexhtml) [16 17] Rarefactionanalysis was implemented based on MOTHUR packageusing operational taxonomic units (OTUs) grouped at 97sequences similarity [18] The numbers of randomly selectedsequences and corresponding OTUs under the sobs diversityindex were employed as the variables

3 Results and Discussion

The soil provides a great variety of microhabitats for myriadorganisms of different size physiological activity behaviorand ecosystem function [19] The extent of the diversityof microorganisms in soil is critical to the maintenanceof health and quality of soil and plant as a wide rangeof microorganisms is involved in important soil functions[20] Recently there have been a few studies on reports ofginger diseases [14 15 21 22] However to the best of ourknowledge the reports on soil microbes in ginger fields arelimited In the present study we compared the microbialdiversity from soil samples of ginger-planting field (gingerwith low disease incidence [healthy sample] versus gingerwith high disease incidence [unhealthy sample]) The dataof this present study showed that both bacterial and fungalOTUs were significantly more in the healthy soil samplethan the unhealthy sample (Table 1) These findings wereconsistent with the previous study about microbial diversityin the soil under cultivation of potato [23] and maize [24]

Scientifica 3

100

80

60

40

20

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ive a

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()






4 Conclusions





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4 Scientifica

Acknowledgments


References







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Journal of




Agronomy





Microbiology

























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4 Conclusions





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4 Scientifica

Acknowledgments


References







2

























Journal of




Agronomy





Microbiology

























4 Scientifica

Acknowledgments


References







2

























Journal of




Agronomy





Microbiology



























Journal of




Agronomy





Microbiology

























Analysis of Microbial Diversity in Soil under Ginger Cultivation...microbe and microbe-ginger...

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