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Soil type influence nutrient availability, microbial metabolic diversity, eubacterial and diazotroph abundance in chickpea rhizosphere

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Abstract

Rhizosphere microbial communities are dynamic and play a crucial role in diverse biochemical processes and nutrient cycling. Soil type and cultivar modulate the composition of rhizosphere microbial communities. Changes in the community composition significantly alter microbial function and ecological process. We examined the influence of soil type on eubacterial and diazotrophic community abundance and microbial metabolic potential in chickpea (cv. BG 372 and cv. BG 256) rhizosphere. The total eubacterial and diazotrophic community as estimated through 16 S rDNA and nifH gene copy numbers using qPCR showed the soil type influence with clear rhizosphere effect on gene abundance. PLFA study has shown the variation in microbial community structure with different soil types. Differential influence of soil types and cultivar on the ratio of Gram positive to Gram negative bacteria was observed with most rhizosphere soils corresponding to higher ratios than bulk soil. The rhizosphere microbial activities (urease, dehydrogenase, alkaline phosphatase and beta-glucosidase) were also assessed as an indicator of microbial metabolic diversity. Principal component analysis and K-means non-hierarchical cluster mapping grouped soils into three categories, each having different soil enzyme activity or edaphic drivers. Soil type and cultivar influence on average substrate utilization pattern analyzed through community level physiological profiling (CLPP) was higher for rhizosphere soils than bulk soils. The soil nutrient studies revealed that both soil type and cultivar influenced the available N, P, K and organic carbon content of rhizosphere soil. Our study signifies that soil type and cultivar jointly influenced soil microbial community abundance and their metabolic potential in chickpea rhizosphere.

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References

  • Ai C, Liang G, Sun J, Wang X, Zhou W (2012) Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma 174(2):330–338

    Article  CAS  Google Scholar 

  • Al-Dhabaan FAM, Bakhali AH (2017) Analysis of the bacterial strains using Biolog plates in the contaminated soil from Riyadh community. Saudi J Bio Sci 24(4):901–906

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. CanJ Biochem Physiol 37(8):911–917

    Article  CAS  Google Scholar 

  • Bray SR, Kitajima K, Mack MC (2012) Temporal dynamics of microbial communities on decomposing leaf litter of 10 plant species in relation to decomposition rate. Soil Biol Biochem 49:30–37

    Article  CAS  Google Scholar 

  • Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841

    Article  CAS  Google Scholar 

  • Casida LE (1977) Microbial metabolic activity in soil as measured by dehydrogenase determinations. Soil Sci 34(6):630–636

    CAS  Google Scholar 

  • Chekanai V, Chikowoa R, Vanlauwe B (2018) Response of common bean (Phaseolus vulgaris L.) to nitrogen, phosphorus and rhizobia inoculation across variable soils in Zimbabwe. Agric Ecosyst Environ 266:167–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ, Tian YH, Zhang Y, Song BR, Li HC, Chen ZH (2016) Effects of root organic exudates on rhizosphere microbes and nutrient removal in the constructed wetlands. Ecol Eng 92:243–250

    Article  Google Scholar 

  • Chen J, Shen W, Xu H, Li Y, Luo T (2019) The Composition of nitrogen-fixing microorganisms correlates with soil nitrogen content during reforestation: a comparison between legume and non-legume plantations. Front Microbiol 10:508

    Article  PubMed  PubMed Central  Google Scholar 

  • Collavino MM, Tripp HJ, Frank IE, Vidoz ML, Calderoli PA, Donato M, Zehr JP, Aguilar OM (2014) nifH pyrosequencing reveals the potential for location-specific soil chemistry to influence N2‐fixing community dynamics. Environ Microbiol 16(10):3211–3223

    Article  CAS  PubMed  Google Scholar 

  • Da Silva KRS, Salles JF, Seldin L, d Van Elsas JD, (2003) Application of a novel Paenibacillus-specific PCR-DGGE method and sequence analysis to assess the diversity of Paenibacillus spp. in the maize rhizosphere. J Microbiol Methods 54:213–231

    Article  PubMed  CAS  Google Scholar 

  • Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt M (2015) Evolution of bacterial communities in the wheat crop rhizosphere. Environ Microbiol 17(3):610–621

    Article  PubMed  Google Scholar 

  • Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606

    Article  CAS  Google Scholar 

  • Fan K, Cardona C, Li Y, Shi Y, Xiang X, Shen C, Wang H, Gilbert JA, Chu H (2017) Rhizosphere-associated bacterial network structure and spatial distribution differ significantly from bulk soil in wheat crop fields. Soil Biol Biochem 113:275–284

    Article  CAS  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. PNAS 103(3):626–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71(7):4117–4120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frostegard A, Tunlid A, Baath E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–163

    Article  Google Scholar 

  • Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28:213–221

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge Y, Zhang JB, Zhang LM, Yang M, He JZ (2008) Long-term fertilization regimes affect bacterial community structure and diversity of an agricultural soil in northern China. J Soils Sediment 8(1):43–50

    Article  CAS  Google Scholar 

  • Gich FB, Amer E, Figueras JB, Abella CA, Balaguer MD, Poch M (2000) Assessment of microbial community structure changes by amplified ribosomal DNA restriction analysis (ARDRA). Internatl Microbiol 3:103–106

    CAS  Google Scholar 

  • Graner G, Persson P, Meijer J, Alstrom S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 29:269–276

    Article  CAS  Google Scholar 

  • Grayston SJ, Vaughan D, Jones D (1997) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5(1):29–56

    Article  Google Scholar 

  • Guckert JB, White DC (1986) Phospholipid ester-linked fatty acid analysis in microbial ecology. In: Megusar F, Kantar G (eds) Perspectives in microbial ecology, Proc Fourth Int Symp Microb Ecol Ljubljana. American Society for Microbiology, Washington, pp 455–459

    Google Scholar 

  • Gupta VSR, Zhang B, Penton CR, Yu J, Tiedje JM (2019) Diazotroph Diversity and Nitrogen Fixation in Summer Active Perennial Grasses in a Mediterranean Region Agricultural Soil. FrontMolBioSci 6:115. https://doi.org/10.3389/fmolb.2019.00115

    Article  CAS  Google Scholar 

  • Hu Y, Xiang D, Veresoglou SD, Chen F, Chen Y, Hao Z, Zhang X, Chen B (2014) Soil organic carbon and soil structure are driving microbial abundance and community composition across the arid and semi-arid grasslands in northern China. Soil Biol Biochem 77:51–57

    Article  CAS  Google Scholar 

  • Inceoglu O, Salles JF, van Elsas JD (2012) Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microbial Ecol 63(2):460–470

    Article  CAS  Google Scholar 

  • Jackson ML (1973) Soil Chemical Analysis, 1st edn. Prentice Hall of India Private Limited, New Delhi

    Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33

    Article  CAS  Google Scholar 

  • Kaur A, Chaudhary A, Kaur A, Choudhary R, Kaushik R (2005) Phospholipid fatty acid a bio indicator of environment monitoring and assessment in soil ecosystem. Curr Sci 89:1103–1112

    CAS  Google Scholar 

  • Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J … Kim JF (2018) Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol 36(11):1100–1109

    Article  CAS  Google Scholar 

  • Liu F, Hewezi T, Lebeis SL, Pantalone V, Grewal PS, Staton ME (2019) Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. BMC Microbiol 19(1):1–19

    Article  Google Scholar 

  • Lundberg DS, Teixeira PJ (2018) Root-exuded coumarin shapes the root microbiome. PNAS 115(22):5629–5631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Mendes R, Kruijt M, De Bruijn I, Dekkers E, van der Voort M, Schneider JH, … Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332(6033):1097–1100

    Article  CAS  PubMed  Google Scholar 

  • Miller KM, Ming TJ, Schulze AD, Withler RE (1999) Denaturing gradient gel electrophoresis (DGGE): a rapid and sensitive technique to screen nucleotide sequence variation in populations. BioTechniques 27:1016–1030

    Article  CAS  PubMed  Google Scholar 

  • Milling A, Smalla K, Xaver F, Maidl K, Schloter M, Munch JC (2004) Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant Soil 266:23–39

    Article  CAS  Google Scholar 

  • Monchgesang S, Strehmel N, Schmidt S, Westphal L, Taruttis F, Muller E, Herklotz S, Newmann S, Scheel D (2016) Natural variation of root exudates in Arabidopsis thaliana-linking metabolomic and genomic data. Sci Rep 6:29033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Naik SKS, Annapurna K, Kumari A, Vithal L, Reddy KK, Swarnalakshmi K (2017) Soybean (Glycine Max) genotype-mediated variation in the symbiotic performance of Rhizobium. Indian J Agric Sci 87(8):1051–1054

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Phosphorus in action. Springer, Berlin, pp 215–243

    Chapter  Google Scholar 

  • Neumann G, Romheld V (2002) Root-induced changes in the availability of nutrients in the rhizosphere. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, third edn. Marcel Dekker, Inc, New York, pp 617–649

    Chapter  Google Scholar 

  • Newton PCD (2013) A reduced fraction of plant N derived from atmospheric N (%Ndfa) and reduced rhizobial nifH gene numbers indicate a lower capacity for nitrogen fixation in nodules of white clover exposed to long-term CO2 enrichment. Biogeosci 10:8269–8281

    Article  CAS  Google Scholar 

  • Nichols D (2007) Cultivation gives context to the microbial ecologist. FEMS Microbiol Ecol 60(3):351–357

    Article  CAS  PubMed  Google Scholar 

  • Olsen S, Cole C, Watanabe F, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular Nr 939. US Gov. Print. Office, Washington

    Google Scholar 

  • Pereira-e-Silva MC, Semenov AV, van Elsas JD, Salles JF (2011) Seasonal variation in diversity and abundance of diazotrophic communities across soils. FEMS Microbiol Ecol 77:57–68

    Article  CAS  PubMed  Google Scholar 

  • Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T (2016) The interaction between iron nutrition, plant species and soil type shapes the rhizosphere microbiome. Plant Physiol Biochem 99:39–48

    Article  CAS  PubMed  Google Scholar 

  • Piotrowska-Dlugosz A, Charzynski P (2015) The impact of the soil sealing degree on microbial biomass, enzymatic activity, and physicochemical properties in the ekranic technosols of toruń (poland). J Soils Sediments 15:47–59

    Article  Google Scholar 

  • Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

    Article  CAS  PubMed  Google Scholar 

  • Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilization profiles-a critique. FEMS Microbiol Ecol 42:1–14

    CAS  PubMed  Google Scholar 

  • Qiao Q, Wang F, Zhang J, Chen Y, Zhang C, Liu G, … Zhang J (2017) The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Sci Rep 7(1):1–10

    Article  CAS  Google Scholar 

  • Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Ann Rev Phytopathol 53:403–424

    Article  CAS  Google Scholar 

  • Rutgers M, Wouterse M, Drost SM, Breure AM, Mulder C, Stone D (2016) Monitoring soil bacteria with community-level physiological profiles using Biolog ECO-plates in the Netherlands and Europe. Appl Soil Ecol 97:23–35

    Article  Google Scholar 

  • Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23(1):25–41

    Article  CAS  PubMed  Google Scholar 

  • SatyaPrakash C, Annapurna K (2006) Diversity of soybean bradyrhizobial population adapted to an Indian soil. J Plant Bio chem Biotechnol 15:27–32

  • Sharma R, Pooniya V, Bisaria VS, Swarnalakshmi K, Sharma S (2020) Bioinoculants play a significant role in shaping the rhizospheric microbial community: a field study with Cajanus cajan. World J Microbiol Biotechnol 36(3):1–17

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith JL, Doran JW (1996) Measurement and use of pH and electrical conductivity for soil quality analysis. In: Doran JW, Jones AJ (eds) Methods for assessing soil quality. Soil Science Society of America Inc. Madison, Wisconsin, USA, pp 169–186

  • Subbiah B, Asija G (1956) A rapid procedure for the estimation of available nitrogen in soils. Curr Sci 25:259–260

    CAS  Google Scholar 

  • Swarnalakshmi K, Annapurna K (2019) Compositional changes of bacterial communities associated with field grown chickpea. Regional Young Investigators’ meeting held at NIPGR, New Delhi during August 6–7, 2019

  • Swarnalakshmi K, Yadav V, Tyagi D, Dhar DW, Kannepalli A, Kumar S (2020) Significance of plant growth promoting rhizobacteria in grain legumes: growth promotion and crop production. Plants 9(11):1596

    Article  CAS  PubMed Central  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1972) Assay of urease activity in soils. Soil Biol Biochem 4:479–487

    Article  CAS  Google Scholar 

  • Treseder KK (2008) Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecol Lett 11(10):1111–1120

    Article  PubMed  Google Scholar 

  • Utobo EB, Tewari L (2015) Soil enzymes as bioindicators of soil ecosystem status. ApplEcol Environ Res 13:147–169

    Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An Extraction method for measuring soil microbial biomass carbon. Soil Biol Biochem 19:703–704

    Article  CAS  Google Scholar 

  • Walkley AJ, Black IA (1934) Estimation of soil organic carbon by the chromic acid titration method. Soil Sci 37:29–38

    Article  CAS  Google Scholar 

  • Walley FL, Boahen SK, Hnatowich G, Stevenson C (2005) Nitrogen and phosphorous fertility management for desi and kabuli chickpea. Can J Plant Sci 85:73–79

    Article  Google Scholar 

  • White DC, Stair JO, Ringelberg DB (1996) Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol Biotechnol 17:185–196

    Article  CAS  Google Scholar 

  • Yuen SH, Pollard AG (1953) Determination of nitrogen in soil and plant materials: Use of boric acid in the micro-kjeldahl method. J Sci Food Agric 4:490–496

    Article  CAS  Google Scholar 

  • Zachow C, Tilcher R, Berg G (2008) Sugar beet-associated bacterial and fungal communities show a high indigenous antagonistic potential against plant pathogens. Microbial Ecol 55(1):119–129

    Article  Google Scholar 

  • Zhao S, Lic K, Zhoua W, Qiua S, Huanga S, Hea P (2016) Changes in soil microbial community, enzyme activities and organic matter fractions under long-term straw return in north-central China. Agric Ecosyst Environ 216:82–88

    Article  CAS  Google Scholar 

  • Zhu X, Zhu B (2015) Diversity and abundance of soil fauna as influenced by long-term fertilization in cropland of purple soil, China. Soil Tillage Res 146:39–46

    Article  Google Scholar 

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Acknowledgements

We acknowledge the Indian Council of Agricultural Research (ICAR) funded projects ICAR-AINP Research Program on Soil diversity and biofertilizer and ICAR-BNF project for sponsoring this research. SG gratefully acknowledges the help for BIOLOG facility provided by Dr. Devyani Tipre, Department of Microbiology & Biotechnology, Gujarat University, India.

Funding

This article was funded by Indian Council of Agricultural Research with Grant Nos. 21-47 and 21-30.

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  1. Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    G. R. Sneha, Karivaradharajan Swarnalakshmi, Meenakshi Sharma, Kedharnath Reddy, Archna Suman & Annapurna Kannepalli

  2. ICAR-IndianAgricultural Statistical Research Institute, New Delhi, 110012, India

    Arpan Bhoumik

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  1. G. R. Sneha
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Sneha, G.R., Swarnalakshmi, K., Sharma, M. et al. Soil type influence nutrient availability, microbial metabolic diversity, eubacterial and diazotroph abundance in chickpea rhizosphere. World J Microbiol Biotechnol 37, 167 (2021). https://doi.org/10.1007/s11274-021-03132-0

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