Skip to main content

Advertisement

SpringerLink
Log in

Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The use of organic compost combined with inorganic fertilizer can enable balanced fertilization under intensive farming conditions, but little is known about how these fertilization practices affect the composition of microbial in arable soils. In this study, a field trial of a rice–wheat cropping system was established to examine the effects of 8 years of fertilization with inorganic fertilizers (IFs) and the organic manure–inorganic fertilizers (OMIFs) on composition of microbial communities. The fungal 18S and bacterial 16S rRNA gene fragments were amplified from each soil sample and sequenced. Significantly lower fungal richness and higher bacterial richness were observed for the OMIF treatment compared to the other treatments. No obvious changes in fungal diversity were observed among the treatments, with a decrease bacterial diversity detected in the IF treatment. Variations in relative abundance were observed in the fungal phyla Glomeromycota, Blastocladiomycota, and Schizoplasmodiida and in the bacterial phyla Acidobacteria, Gemmatimonadetes, and Cyanobacteria, most of which were significantly correlated with soil organic matter (OM) and/or nitrate N (NO3 −-N) contents. Additionally, the fungal abundance-based coverage estimator (ACE) showed a significant negative correlation with the soil NO3 −-N/OM content, while the correlation was positive for the bacterial ACE estimate. This study suggests that the fungal and bacterial communities respond differently to the long-term organic-inorganic fertilization, which may result from different effects of NO3 −-N/OM content of soil on the composition of fungal and bacterial communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acosta-Martinez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770

    Article  CAS  Google Scholar 

  • Bansal S, Kapoor KK (2000) Vermicomposting of crop residues and cattle dung with Eisenia foetida. Bioresour Technol 73:95–98

    Article  CAS  Google Scholar 

  • Börjesson G, Menichetti L, Kirchmann H, Kätterer T (2012) Soil microbial community structure affected by 53 years of nitrogen fertilisation and different organic amendments. Biol Fert Soils 48:245–257

    Article  Google Scholar 

  • Bremner JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL (ed) Methods of soil analysis, part 2. Chemical and microbiological properties, vol 9, Agronomy No. ASA, SSSA, Madison, pp 595–624

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 1:4516–4522

    Article  Google Scholar 

  • Chen M, Cui Y, Bai F, Wang J (2013) Effect of two biogas residues application on copper and zinc fractionation and release in different soils. J Environ Sci (China) 25:1865–1873

    Article  CAS  Google Scholar 

  • Chen YL, Zhang X, Ye JS, Han HY, Wan SQ, Chen BD (2014) Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in Inner Mongolia. Soil Biol Biochem 69:371–381

    Article  CAS  Google Scholar 

  • Chu H, Lin X, Fujii T, Morimoto S, Yagi K, Hu JL, Zhang J (2007) Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol Biochem 39:2971–2976

    Article  CAS  Google Scholar 

  • Corkidi L, Rowland DL, Johnson NC, Allen EB (2002) Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grasslands. Plant Soil 240:299–310

    Article  CAS  Google Scholar 

  • Cui ZL, Yue SC, Wang GL, Meng QF, Wu L, Yang ZP, Li SQ, Zhang FS, Chen XP (2013) Closing the yield gap could reduce projected greenhouse gas emissions: a case study of maize production in China. Glob Chang Biol 19:2467–2477

    Article  PubMed  Google Scholar 

  • Dawe D, Frolking S, Li C (2004) Trends in rice-wheat area in China. Field Crops Res 87:89–95

    Article  Google Scholar 

  • DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microb 77:6295–6300

    Article  CAS  Google Scholar 

  • Delmont TO, Francioli D, Jacquesson S, Laoudi L, Mathieu A, Nesme J, Ceccherini MT, Nannipieri P, Simonet P, Vogel TM (2014) Microbial community development and unseen diversity recovery in inoculated sterile soil. Biol Fertil Soils 50:1069–1076

    Article  CAS  Google Scholar 

  • Ebhin MR, Chhonkar P, Singh D, Patra A (2006) Changes in soil biological and biochemical characteristics in a long-term field trial on a sub-tropical inceptisol. Soil Biol Biochem 38:1577–1582

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496

    Article  Google Scholar 

  • Eneji AE, Yamanioto S, Honna T, Ishiguro A (2001) Physicochemical changes in livestock feces during composting. Commun Soil Sci Plant Anal 32:477–489

    Article  CAS  Google Scholar 

  • Etten EV (2005) Multivariate analysis of ecological data using CANOCO. Austral Eco 30:486–487

    Article  Google Scholar 

  • Ge G, Li Z, Fan F, Chu G, Hou Z, Liang YC (2010) Soil biological activity and their seasonal variations in response to long-term application of organic and inorganic fertilizers. Plant Soil 326:31–44

    Article  CAS  Google Scholar 

  • Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms—a review. Soil Biol Biochem 75:54–63

    Article  CAS  Google Scholar 

  • Guo LJ, Zhang ZS, Wang DD, Li CF, Cao CG (2015) Effects of short-term conservation management practices on soil organic carbon fractions and microbial community composition under a rice-wheat rotation system. Biol Fertil Soils 51:65–75

    Article  CAS  Google Scholar 

  • Haynes RJ, Naidu R (1998) Influence of lime, fertilizer and manure applications on soil organic matter content and soil physical conditions: a review. Nutr Cycl in Agroecosys 51:123–137

    Article  Google Scholar 

  • Helgason BL, Walley FL, Germida JJ (2010) Long-term no-till management affects microbial biomass but not community composition in Canadian prairie agroecosytems. Soil Biol Biochem 42:2192–2202

    Article  CAS  Google Scholar 

  • Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S (2013) Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc Natl Acad Sci U S A 110:11911–11916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam MR, Chauhan PS, Kim Y, Kim M, Sa T (2011) Community level functional diversity and enzyme activities in paddy soils under different longterm fertilizer management practices. Biol Fert Soils 47:599–604

    Article  Google Scholar 

  • Joergensen RG, Mäder P, Fließbach A (2010) Long-term effects of organic farming on fungal and bacterial residues in relation to microbial energy metabolism. Biol Fertil Soils 46:303–307

    Article  CAS  Google Scholar 

  • Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908

    Article  Google Scholar 

  • Jones MD, Phillips LA, Treu R, Ward V, Berch SM (2012) Functional responses of ectomycorrhizal fungal communities to long-term fertilization of lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm.) stands in central British Columbia. Appl soil Ecol 60:29–40

    Article  Google Scholar 

  • 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. Proc Natl Acad Sci U S A 106:3041–3046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12:1–15

    Article  CAS  Google Scholar 

  • Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25

    Article  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75:5111–5120

    Article  CAS  Google Scholar 

  • Lazcano C, Brandón-Gómez M, Revilla P, Domínguez J (2013) Shortterm effects of organic and inorganic fertilizers on soil microbial community structure and function. Biol Fertil Soils 49:723–733

    Article  CAS  Google Scholar 

  • Lee CK, Barbier BA, Bottos EM, McDonald IR, Cary SC (2012) The inter-valley soil comparative survey: the ecology of Dry Valley edaphic microbial communities. ISME J 6:1046–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Zhang Y, Han W, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Shi G, Mao L, Cheng G, Jiang S, Ma X, An L, Du G, Collins Johnson N, Feng H (2012) Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523–535

    Article  CAS  PubMed  Google Scholar 

  • Lv M, Li Z, Che Y, Han F, Liu M (2011) Soil organic C, nutrients, microbial biomass, and grain yield of rice (Oryza sativa L.) after 18 years of fertilizer application to an infertile paddy soil. Biol Fert Soils 47:777–783

    Article  CAS  Google Scholar 

  • Miransari M (2011) Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl Microbiol Biotechnol 89:917–930

    Article  CAS  PubMed  Google Scholar 

  • Merwin HD, Peech M (1950) Exchangeability of soil potassium in sand, silt and clay fractions as influenced by the nature of the complementary cation. Soil Sci Soc Am J 15:125–128

    Article  Google Scholar 

  • Murugan R, Kumar S (2013) Influence of long-term fertilisation and crop rotation on changes in fungal and bacterial residues in a tropical ricefield soil. Biol Fertil Soils 49:847–856

    Article  Google Scholar 

  • Ogilvie LA, Hirsch PR, Johnston AWB (2008) Bacterial diversity of the Broadbalk ‘classical’ winter wheat experiment in relation to long-term fertilizer inputs. Microbial Ecol 56:525–537

    Article  Google Scholar 

  • Paungfoo-Lonhienne C, Yeoh YK, Kasinadhuni NRP, Lonhienne TG, Robinson N, Hugenholtz P, Ragan MA, Schmidt S (2015) Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci Rep 5:8678

    Article  CAS  PubMed  Google Scholar 

  • Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2007) Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant Soil 296:65–75

    Article  CAS  Google Scholar 

  • Poulsen PH, Al-Soud WA, Bergmark L, Magid J, Hansen LH, Sørensen SJ (2013) Effects of fertilization with urban and agricultural organic wastes in a field trial–Prokaryotic diversity investigated by pyrosequencing. Soil Biol Biochem 57:784–793

    Article  CAS  Google Scholar 

  • Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Global Change Biol 18:1918–1927

    Article  Google Scholar 

  • Rivas S, Thomas CM (2005) Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu Rev Phytopathol 43:395–436

    Article  CAS  PubMed  Google Scholar 

  • Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, Daroub SH, Camargo FA, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ros M, Pascual JA, Garcia C, Hernandez MT, Insam H (2006) Hydrolase activities, microbial biomass and bacterial community in a soil after long-term amendment with different composts. Soil Biol Biochem 38:3443–3452

    Article  CAS  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • 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 Microb 75:7537–7541

    Article  CAS  Google Scholar 

  • Schönning C, Leeming R, Stenström TA (2002) Faecal contamination of source separated human urine based on the content of faecal sterols. Water Res 36:1965–1972

    Article  PubMed  Google Scholar 

  • Shen Z, Ruan Y, Chao X, Zhang J, Li R, Shen Q (2015) Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fertil Soils 51:553–562

    Article  CAS  Google Scholar 

  • Singh BK, Campbell CD, Sorenson SJ, Zhou J (2009) Soil genomics. Nat Rev Microbiol 7:756–756

    Article  CAS  PubMed  Google Scholar 

  • Steiner C, Teixeira WG, Lehmann J, Nehls T, de Macêdo JLV, Blum WEH, Zech W (2007) Long term effects of manure, charcoal and mineral fertilization on crop production and fertility on a highly weathered Central Amazonian upland soil. Plant Soil 291:275–290

    Article  CAS  Google Scholar 

  • Usman ARA, Kuzyakov Y, Stahr K (2004) Dynamics of organic C mineralization and the mobile fraction of heavy metals in a calcareous soil incubated with organic wastes. Water Air Soil Poll 158:401–418

    Article  CAS  Google Scholar 

  • Van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM (2007) Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytol 176:175–183

    Article  PubMed  Google Scholar 

  • Wargo MJ, Hogan DA (2006) Fungal—bacterial interactions: a mixed bag of mingling microbes. Curr Opin Microbiol 9:359–364

    Article  CAS  PubMed  Google Scholar 

  • Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci Soc Am J 29:677–678

    Article  CAS  Google Scholar 

  • Yeomans JC, Bremner JM (1988) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plant 19:1467–1476

    Article  CAS  Google Scholar 

  • Yin C, Hulbert SH, Schroeder KL, Mavrodi O, Mavrodi D, Dhingra A (2013) Role of bacterial communities in the natural suppression of Rhizoctonia solani bare patch of wheat (Triticum aestivum L.). Appl Environ Microb 79:7428–7438

    Article  CAS  Google Scholar 

  • Zhang H, Ding W, Yu H, He X (2015) Linking organic carbon accumulation to microbial community dynamics in a sandy loam soil: result of 20 years compost and inorganic fertilizers repeated application experiment. Biol Fertil Soils 51:137–150

    Article  CAS  Google Scholar 

  • Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Zhang R (2014) Responses of bacterial communities in arable soils in a rice-wheat cropping system to different fertilizer regimes and sampling times. Plos One 9:e85301

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhong W, Cai Z (2007) Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl Soil 36:84–91

    Article  Google Scholar 

Download references

Acknowledgment

This work was funded by the National Natural Science Foundation of China (41571307); the Science Foundation of Jiangsu Province, China (BE2014742).

Author information

Authors and Affiliations

  1. College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Chen Chen, Jianan Zhang, Min Lu, Chun Qin, Yahua Chen & Zhenguo Shen

  2. Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Chen Chen, Chun Qin, Yahua Chen, Qiwei Huang, Jichen Wang, Zhenguo Shen & Qirong Shen

  3. Jiangsu Provincial Key Laboratory of Coastal Wetland Bioresources and Environmental Protection, Yancheng Teachers University, Yancheng, 224002, People’s Republic of China

    Li Yang

Authors
  1. Chen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chun Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yahua Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qiwei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jichen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhenguo Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qirong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenguo Shen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 399 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, C., Zhang, J., Lu, M. et al. Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biol Fertil Soils 52, 455–467 (2016). https://doi.org/10.1007/s00374-016-1089-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-016-1089-5

Keywords

Search

Navigation