Abstract
The association between microbial communities and plant growth in long-term fertilization system has not been fully studied. In the present study, impacts of long-term fertilization have been determined on the size and activity of soil microbial communities and wheat performance in a red soil (Ultisol) collected from Qiyang Experimental Station, China. For this, different microbial communities originating from long-term fertilized pig manure (M), mineral fertilizer (NPK), pig manure plus mineral fertilizer (MNPK), and no fertilizer (CK) were used as inocula for the Ultisol tested. Changes in total bacterial and fungal community composition and structures using Ion Torrent sequencing were determined. The results show that the biomass of wheat was significantly higher in both sterilized soil inoculated with NPK (SNPK) and sterilized soil inoculated with MNPK (SMNPK) treatments than in other treatments (P < 0.05). The activities of β-1,4-N-acetylglucosaminidase (NAG) and cellobiohydrolase (CBH) were significantly correlated with wheat biomass. Among the microbial communities, the largest Ascomycota phylum in soils was negatively correlated with β-1,4-glucosidase (βG) (P < 0.05). The phylum Basidiomycota was negatively correlated with plant biomass (PB) and tillers per plant (TI) (P < 0.05). Nonmetric multidimensional scaling analysis shows that fungal community was strongly correlated with long-term fertilization strategy, while the bacterial community was strongly correlated with β-1,4-N-acetylglucosaminidase activity. According to the Mantel test, the growth of wheat was affected by fungal community. Taken together, microbial composition and diversity in soils could be a good player in predicting soil fertility and consequently plant growth.
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Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vralstad T, Liimatainen K, Peintner U, Koljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285
Adams RI, Amend AS, Taylor JW, Bruns TD (2013) Distorts the perception of species richness and composition in high-throughput sequencing surveys of microbial communities: a case study of fungi in indoor dust. Microb Ecol 66(4):735–741
Ashton IW, Miller AE, Bowman WD, Suding KN (2008) Nitrogen preferences and plant–soil feedbacks as influenced by neighbors in the alpine tundra. Oecologia 156:625–636
Bainard LD, Koch AM, Gordon AM, Klironomos JN (2013) Growth response of crops to soil microbial communities from conventional monocropping and tree-based intercropping systems. Plant Soil 363:345–356
Bender SF, van der Heijden MGA (2015) Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J Appl Ecol 52:228–239
Bever JD (2002) Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290
Bhattacharyya P, Chakrabarti K, Chakraborty A (2005) Microbial biomass and enzyme activities in submerged rice soil amended with municipal solid waste compost and decomposed cow manure. Chemosphere 60:310–318
Biddle AS, Black SJ, Blanchard JL (2013) An in vitro model of the horse gut microbiome enables identification of lactate-utilizing bacteria that differentially respond to starch induction. PLoS ONE 8 (10):e77599
Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058
Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soilmicrobial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12
Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setälä H, Staddon PL, Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298:615–618
Brinkman EP, van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073
Crecchio C, Curci M, Pellegrino A, Ricciuti P, Tursi N, Ruggiero P (2007) Soil microbial dynamics and genetic diversity in soil under monoculture wheat grown in different long-term management systems. Soil Biol Biochem 39:1391–1400
Dassi E, Ballarini A, Covello G, Quattrone A, Jousson O, De Sanctis V, Bertorelli R, Denti MA, Segata N (2014) Enhanced microbial diversity in the saliva microbiome induced by short-term probiotic intake revealed by 16S rRNA sequencing on the Ion Torrent PGM platform. J Biotechnol 190:30–39
Davey ML, Heegaard E, Halvorsen R, Ohlson M, Kauserud HM (2012) Seasonal trends in the biomass and structure of bryophyte-associated fungal communities explored by 454 pyrosequencing. New Phytol 195(4):844–856
Elgersma K, Ehrenfeld J, Yu S, Vor T (2011) Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167:733–745
Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microb 71:8335–8343
Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol S 42:23–46
Ge GF, Li ZJ, Zhang J, Wang LG, Xu MG, Zhang JB, Wang JK, Xie XL, Liang YC (2009) Geographical and climatic differences in long-term effect of organic and inorganic amendments on soil enzymatic activities and respiration in field experimental stations of China. Ecol Complex 6:421–431
Gómez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, van Beusekom JEE, Amann R (2010) Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4(4):472–487
Gu Y, Zhang X, Tu S, Lindström K (2009) Soil microbial biomass, crop yields, and bacterial community structure as affected by long-term fertilizer treatments under wheat-rice cropping. Eur J Soil Biol 45:239–246
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374
He JZ, Zheng Y, Chen CR, He YQ, Zhang LM (2008) Microbial composition and diversity of an upland red soil under long-term fertilization treatments as revealed by culture-dependent and culture-independent approaches. J Soils Sediments 8:349–358
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Lumbsch HT, Lutzoni F, Matheny PB, Mclaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüssler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547
Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308
Ibekwe AM, Kennedy AC, Frohne PS, Papiernik SK, Yang C-H, Crowley DE (2002) Microbial diversity along a transect of agronomic zones. FEMS Microbiol Ecol 39(3):183–191
Ju XT, Xing GX, Chen XP, Zhang SL, Zhang LJ, Liu XJ, Cui ZL, Yin B, Christie P, Zhu ZL, Zhang FS (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. P Natl Acad Sci USA 106(9):3041–3046
Keiser AD, Strickland MS, Fierer N, Bradford MA (2011) The effect of resource history on the functioning of soil microbial communities is maintained across time. Biogeosciences Discuss 8:1643–1667
Kuramae EE, Gamper HA, Yergeau E, Piceno YM, Brodie EL, DeSantis TZ, Andersen GL, van Veen JA, Kowalchuk GA (2010) Microbial secondary succession in a chronosequence of chalk grasslands. ISME J 4:711–715
Ladd JN, Amato M, Zhou LK, Schultz JE (1994) Differential effect of rotation, plant residue and nitrogen fertilizer and microbial biomass and organic matter in an Australian alfisol. Soil Biol Biochem 26:821–831
Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars KM, Smit E (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69(1):327–333
Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. P Natl Acad Sci USA 109:14058–14062
Lee WJ, Wood CW, Reeves DW, Entry JA, Raper RL (1996) Interactive effects of wheel-traffic and tillage system on soil carbon and nitrogen. Commun Soil Sci Plant Anal 27:3027–3043
Ling N, Sun Y, Ma J, Guo J, Zhu P, Peng C, Yu G, Ran W, Guo S, Shen Q (2014) Response of the bacterial diversity and soil enzyme activity in particle-size fractions of Mollisol after different fertilization in a long-term experiment. Biol Fert Soils 50:901–911
Lou Y, Sharon AC, Adam SD, Anita D, Joel F, Analiza HMR, Christy LS, Anthony CY (2014) An affinity–effect relationship for microbial communities in plant–soil feedback loops. Microb Ecol 67:866–876
Lupwayi NZ, Grant CA, Soon YK, Clayton GW, Bittman S, Malhi SS, Zebarth BJ (2010) Soil microbial community response to controlled-release urea fertilizer under zero tillage and conventional tillage. Appl Soil Ecol 45:254–261
Lupwayi NZ, Clayton GW, O’Donovan JT, Grant CA (2011) Soil microbial response to nitrogen rate and placement and barley seeding rate under no till. Agron J 103:1064–1071
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
McCune B, Mefford MJ (1999) PC-ORD for Windows. Multivariate analysis of ecological data. Version 4.01. MjM Software, Gleneden Beach, OR
Mirete S, de Figueras CG, Gonzalez-Pastor JE (2007) Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl Environ Microb 73(19):6001–6011
Mueller GM, Schmit JP, Leacock PR, Buyck B, Cifuentes J, Desjardin DE, Halling RE, Hjortstman K, Iturriaga T, Larsson KH, Lodge DJ, May TW, Minter D, Rajchenberg M, Redhead SA, Ryvarden L, Trappe JM, Watling R, Wu QW (2007) Global diversity and distribution of macrofungi. Biodivers Conserv 16:37–48
Nannipieri P, Giagnoni L, Lagomarsino G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fert Soils 48:743–762
Pansu M, Gautheyrou J (2006) Handbook of soil analysis: mineralogical, organic and inorganic methods. Springer Verlag, Berlin
Parikh SJ, James BR (2012) Soil: the foundation of agriculture. Nature Education Knowledge 3(10):2
Phillips RP, Meier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC (2012) Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol Lett 15:1042–1049
Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an acersaccharum forest soil. Soil Biol Biochem 34:1309–1315
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541
Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611
Tan KH (2005) Soil sampling, preparation, and analysis. CRC Press, Boca Raton
Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Koljalg U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188:291–301
Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66(8):2167–2175
van de Voorde TFJ, van der Putten WH, Bezemer TM (2012) Soil inoculation method determines the strength of plant-soil interactions. Soil Biol Biochem 55:1–6
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310
Verbruggen E, Kiers ET, Bakelaar PNC, Roling WFM, van der Heijden MGA (2012) Provision of contrasting ecosystem services by soil communities from different agricultural fields. Plant Soil 350:43–55
Wei G, Kloepper JW, Tuzun S (1996) Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions. Phytopathology 86:221–224
Whiteley AS, Jenkins S, Waite I, Kresoje N, Payne H, Mullan B, Allcock R, O’Donnell A (2012) Microbial 16S rRNA ion tag and community metagenome sequencing using the Ion Torrent (PGM) Platform. J Microbiol Meth 91:80–88
Wilson M, Backman PA (1999) In: Ruberson JR (ed) Handbook of pest management: biological control of plant pathogens. Marcel Dekker Inc., New York, p 309
Zak DR, Groffman PM, Pregitzer KS, Christensen S, Tiedje JM (1990) The vernal dam: plant-microbe competition for nitrogen in northern hardwood forests. Ecology 71:651–656
Zhang HM, Wang BR, Xu MG, FAN TL (2009) Crop yield and soil responses to long-term fertilization on a red soil in southern China. Pedosphere 19(2):199–207
Acknowledgements
This work was jointly supported by the 12th Five-Year Key Programs for Science and Technology Development of China “Study of Key Technologies for Alleviating Obstacle Factors and Improving Productivity of Low-yield Cropland” (Approved No. 2012BAD05B06), as well as grants from the National Key Basic Research Support Foundation of China (NKBRSF) (Approved No. 2015CB150502) and the National Natural Science Foundation of China (Approved No. 41171208).
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Li, L., Fan, F., Song, A. et al. Microbial composition and diversity are associated with plant performance: a case study on long-term fertilization effect on wheat growth in an Ultisol. Appl Microbiol Biotechnol 101, 4669–4681 (2017). https://doi.org/10.1007/s00253-017-8147-2
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DOI: https://doi.org/10.1007/s00253-017-8147-2