Skip to main content

Advertisement

SpringerLink
Log in

Three decades of organic manure and chemical fertilizers co-application enhanced rice productivity through increasing the diversity and key network module of soil bacterial community

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Soil bacteria play a vital role in crop growth and production. However, the impact of long-term application of chemical fertilizers or combined with organic manure on the soil bacterial communities (diversity, structure, and co-occurrence patterns) and their relationships with rice (Oryza sativa L.) productivity remains unclear.

Methods

A 30-year fertilization trial was conducted in a Chinese paddy field with three treatments of no fertilizer (CK), chemical fertilizer (NPK), chemical fertilizers, and pig manure co-application (NPKM). The co-occurrence network and key species for yield enhancement were investigated in combination with bacterial community structure by high-throughput sequencing.

Results

NPKM treatment significantly increased the contents of carbon, nitrogen, phosphorus, and pH value in the soil. Compared to CK and NPK treatments, NPKM significantly enhanced rice yield by an average of 43.51 and 18.69% in the last 2 years (2019 and 2020). NPKM rather than NPK resulted in a significant increase in bacterial alpha diversity. PCoA showed that both NPKM and NPK substantially shaped bacterial structure. Moreover, three ecological clusters (modules 1, 7, and 9) were observed under the ecological network involving all samples, and modules 1 (negative) and 7 (positive) had strong associations with rice yield. Concretely, Chloroflexi contributed most to the rice yield in module 7. Soil pH, SOM, and TN were the main soil factors affecting bacterial communities and co-occurrence patterns.

Conclusions

These results suggested that long-term organic manure and chemical fertilizer co-application outperforms chemical fertilization in increasing rice productivity through enhancing soil bacterial diversity and harboring more beneficial members in its ecological cluster.

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

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Adeleke BS, Ayangbenro AS, Babalola OB (2021) Bacterial community structure of the sunflower (Helianthus annuus) endosphere. Plant Signal Behav 16:1974217

    Article  Google Scholar 

  • Ahn JH, Lee SA, Kim JM, Kim MS, Song J, Weon HY (2016) Dynamics of bacterial communities in rice field soils as affected by different long-term fertilization practices. J Microbiol 54:724–731

    Article  CAS  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    Article  CAS  Google Scholar 

  • Banerjee S, Schlaeppi K, Heijden MG (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16(9):567–576

    Article  CAS  Google Scholar 

  • Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, Keller T, Charles R, Heijden MG (2019) Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J 13:722–1736

    Article  Google Scholar 

  • Bao SD (2000) Soil agricultural chemical analysis, 3rd edn. Agriculture Press, Beijing (in Chinese)

    Google Scholar 

  • Barberan A, Casamayor OC, Fierer N (2014) The microbial contribution to macroecology. Front Microbiol 5:203

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pea AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Cesarano G, De Filippis F, La Storia A, Scala F, Bonanomi G (2017) Organic amendment type and application frequency affect crop yields, soil fertility and microbiome composition. Appl Soil Ecol 120:254–264

    Article  Google Scholar 

  • Chen D, Xing W, Lan Z, Saleem M, Yunqiqige Wu, Shuijin Hu, Dima YBC, Xing W, Lan Z, Saleem M, Wu YQQG, Hu SJ, Bai YF (2018) Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi-arid grassland. Funct Ecol 33:175–187

    Article  Google Scholar 

  • Chen ZM, Wang HY, Liu XW, Zhao XL, Lu DJ, Zhou JJ, Li CZ (2017) Changes in soil microbial community and organic carbon fractions under short-term straw return in a rice–wheat cropping system. Soil till Res 165:121–127

    Article  Google Scholar 

  • Csárdi G, Nepusz T (2006) The igraph software package for complex network research. Inter Journal, Complex Systems 1695:1–9

    Google Scholar 

  • Cui XW, Zhang YZ, Gao JS, Peng FY, Gao P (2018) Long-term combined application of manure and chemical fertilizer sustained higher nutrient status and rhizospheric bacterial diversity in reddish paddy soil of Central South China. Sci Rep 8:1–11

    Article  Google Scholar 

  • De Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:1–12

    Article  Google Scholar 

  • Degrune F, Dufrêne M, Colinet G, Massart S, Taminiau B, Bodson B, Hiel M-P, Daube G, Nezer C, Vandenbol M (2015) A novel sub-phylum method discriminates better the impact of crop management on soil microbial community. Agron Sustain Dev 35:1157–1166

    Article  Google Scholar 

  • Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359(6373):320–325

  • Deng NY, Grassini P, Yang HS, Huang JL, Cassman KG, Peng SB (2019) Closing yield gaps for rice self-sufficiency in China. Nat Commun 10:1725

    Article  Google Scholar 

  • Diacono M, Montemurro F (2011) Long-term effects of organic amendments on soil fertility. Sustainable Agriculture 2(34):761–786

    Google Scholar 

  • Durrer A, Gumiere T, Zagatto MRG, Henrique PF, Antonio MMS, Rodrigo HL, Sérgio KH, Elke JBN (2021) Organic farming practices change the soil bacteria community, improving soil quality and maize crop yields. PeerJ 9:e11985

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fan KK, Weisenhorn P, Gilbert JA, Chu HY (2018) Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biol Biochem 125:251–260

    Article  CAS  Google Scholar 

  • Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550

    Article  CAS  Google Scholar 

  • Franklin RB, Mills AL (2006) Structural and functional responses of a sewage microbial community to dilution-induced reductions in diversity. Microb Ecol 52:280–288

    Article  Google Scholar 

  • Freilich MA, Wieters E, Broitman BR, Marquet PA, Navarrete SA (2018) Species co-occurrence networks: can they reveal trophic and non-trophic interactions in ecological communities? Ecology 99:690–699

    Article  Google Scholar 

  • Gao B, Ju XT, Zhang Q, Christie P, Zhang FS (2011) New estimates of direct N2O emissions from Chinese croplands from 1980 to 2007 using localized emission factors. Biogeosciences 8:3011–3024

    Article  CAS  Google Scholar 

  • Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KW, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

    Article  CAS  Google Scholar 

  • Harrell FE, Dupont C (2008) Hmisc: harrell miscellaneous. R Package Version 3:437

    Google Scholar 

  • Hartman K, Van D, Wittwer RA, Banerjee S, Walser JC, Schlaeppi K (2018) Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome 6:14

    Article  Google Scholar 

  • Hashmi I, Bindschedler S, Junier P (2020) Firmicutes. New York, USA, pp 363–396

  • He D, Shen WJ, Eberwein J, Zhao Q, Ren LJ, Wu QL (2017) Diversity and co-occurrence network of soil fungi are more responsive than those of bacteria to shifts in precipitation seasonality in a subtropical forest. Soil Biol Biochem 115:499–510

    Article  CAS  Google Scholar 

  • Hu XX, Liu JJ, Wei DP, Zhu P, Cui X, Chen ZBK, XL, Jin J, Liu XB, Wang GH (2018) Soil bacterial communities under different long-term fertilization regimes in three locations across the black soil region of northeast China. Pedosphere 28:751–763

    Article  CAS  Google Scholar 

  • Huang M, Tian A, Chen JN, Cao FB, Chen YM, Liu LS (2020) Soil bacterial communities in three rice-based cropping systems differing in productivity. Sci Rep 10:1–5

    Google Scholar 

  • Igalavithana AD, Lee SS, Niazi NK, Young H (2017) Assessment of soil health in urban agriculture: soil enzymes and microbial properties. Sustainability-Basel 9:310

  • Ikoyi I, Egeter B, Chaves C, Ahmed M, Fowler A, Schmalenberger A (2020) Responses of soil microbiota and nematodes to application of organic and inorganic fertilizers in grassland columns. Bio Fert Soils 56:647–662

    Article  CAS  Google Scholar 

  • Iqbal A, He L, Ali I, Yuan P, Khan A, Hua Z, Wei S, Jiang L (2022) Partial substation of organic fertilizer with chemical fertilizer improves soil biochemical attributes, rice yields, and restores bacterial community diversity in a paddy field. Front Plant Sci 13:895230

    Article  Google Scholar 

  • Jiao S, Lu Y (2020) Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environ Microbiol 22:1052–1065

    Article  Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  CAS  Google Scholar 

  • Kragelund C, Levantesi C, Borger A, Thelen K, Eikelboom D, Tandoi V (2007) Identity, abundance and ecophysiology of filamentous Chloroflexi speciespresent in activated sludge treatment plants. FEMS Microbiol Ecol 59:671–682

    Article  CAS  Google Scholar 

  • Kumar M, Kundu DK, Ghorai A K, Mitra S, Singh SR (2018) Carbon and nitrogen mineralization kinetics as influenced by diversified cropping systems and residue incorporation in Inceptisols of eastern Indo-Gangetic Plain. Soil Till Res 178: 108–117

  • Kumar U, Kumar NA, Shahid M, Gupta VVSR, Panneerselvam P, Mohanty S, Kaviraj M, Kumar A, Chatterjee D, Lal B, Gautam P, Tripathi R, Panda BB (2018) Continuous application of inorganic and organic fertilizers over 47 years in paddy soil alters the bacterial community structure and its influence on rice production. Agr Ecosyst Environ 262:65–75

    Article  Google Scholar 

  • Lal R (2015) Restoring soil quality to mitigate soil degradation. Sustainability-Basel 7:5875–5895

    Article  Google Scholar 

  • Layeghifard M, Hwang DM (2017) Disentangling interactions in the microbiome: a network perspective. Trends Microbiol 25(3):217–228

    Article  CAS  Google Scholar 

  • Li CH, Yan K, Jia TLS, ZJ, Li Y (2014) Change in deep soil microbial communities due to long-term fertilization. Soil Biol Biochem 75:264–272

    Article  CAS  Google Scholar 

  • Li F, Chen L, Zhang JB, Yin J, Huang SM (2017) Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front Microbiol 8:187

    Google Scholar 

  • Li JG, Shen MC, Hou JF, Li L, Wu JX, Dong YH (2016) Effect of different levels of nitrogen on rhizosphere bacterial community structure in intensive monoculture of greenhouse lettuce. Sci Rep 6:25305

    Article  CAS  Google Scholar 

  • Li QS, Chen J, Wu LK, Luo XM, Luo XM, Arafat Y, Lin S, Lin WX (2018) Belowground interactions impact the soil bacterial community, soil fertility, and crop yield in maize/peanut intercropping systems. Int J Mol Sci 19:622

    Article  CAS  Google Scholar 

  • Li X, Zhao YS, Sun GY, Jin WW, Sun ML, Zhang HH, Xu N, Cai DJ, Li DM (2020) Linking soil bacterial community and crop yield in a wheat (Triticum aestivum L.)-alfalfa (Medicago sativa L.) intercropping system. Appl Ecol Env Res 8:4487–4505

    Article  Google Scholar 

  • Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2:18–22

    Google Scholar 

  • Liu C, Cui YM, Li XZ, Yao MJ (2021) Microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol 97:255

    Article  Google Scholar 

  • Liu HY, Huang X, Tan WF, Di HJ, Xu JM, Li Y (2020) High manure load reduces bacterial diversity and network complexity in a paddy soil under crop rotations. Soil Ecol Lett 2:104–119

    Article  CAS  Google Scholar 

  • Lin YX, Ye GP, Kuzyakov Y, Liu DY, Ding WX (2019) Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol Biochem 134:187–196

    Article  CAS  Google Scholar 

  • Ma B, Wang HZ, Dsouza M, Lou J, Xu JA (2015) Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME J 10:1891

    Article  Google Scholar 

  • Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  CAS  Google Scholar 

  • Männistö M, Ganzert L, Tiirola M, Häggblom MM, Stark S (2016) Do shifts in life strategies explain microbial community responses to increasing nitrogen in tundra soil? Soil Biol Biochem 96:216–228

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan.’ Community Ecology Package, Version 2:1–295

    Google Scholar 

  • Qin YS, Wang ZY, Jiaka LT, Tu SH (2010) Cadmium uptake by paddy rice and soil available Cd under water flooding as affected by nitrogen fertilizer. 4th International Conference on Bioinformatics and Biomedical Engineering pp, 1–5

  • Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Oves M (2016) Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res 183:26–41

    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  Google Scholar 

  • Roychowdhury R, Abdel Gawwad MR, Banerjee U, Bishnu S, Tah J (2012) Status, trends and prospects of organic farming in India: a review. J Plant Biol Res 2:38–48

    Google Scholar 

  • Rukshana F, Butterly CR, Baldock JA, Xu JM, Tang C (2012) Model organic compounds differ in priming effects on alkalinity release in soils through carbon and nitrogen mineralisation. Soil Biol Biochem 51:35–43

    Article  CAS  Google Scholar 

  • Sun RB, Zhang XX, Guo XS, Wang DZ, Chu HY (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18

    Article  CAS  Google Scholar 

  • Tian W, Wang L, Li Y, Zhuang KM, Li G, Zhang JB, Xiao XJ, Xi YG (2015) Responses of microbial activity, abundance, and community in wheat soil after three years of heavy fertilization with manure-based compost and inorganic nitrogen. Agr Ecosyst Environ 213:219–227

    Article  CAS  Google Scholar 

  • Treseder KK, Kivlin SN, Hawkes CV (2011) Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecol Lett 14:933–938

    Article  Google Scholar 

  • Vineela C, Wani SP, Srinivasara C, Padmaja B, Vittal KPR (2008) Microbial properties of soils as affected by cropping and nutrient management practices in several long-term manurial experiments in the semi-arid tropics of India. Appl Soil Ecol 40:165–173

    Article  Google Scholar 

  • Walsh JR, Carpenter SR, Vander Zanden MJ (2016) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc Natl Acad Sci USA 113:4081–4085

    Article  CAS  Google Scholar 

  • Wang HX, Xu JL, Liu XJ, Zhang D, Li LW, Li W, Sheng LX (2019) Effects of long-term application of organic fertilizer on improving organic matter content and retarding acidity in red soil from China. Soil till Res 195:104382

    Article  Google Scholar 

  • Wang JL, Liu KL, Zhao XQ, Zhang HQ, Li D, Li JJ, Shen RF (2021) Balanced fertilization over four decades has sustained soil microbial communities and improved soil fertility and rice productivity in red paddy soil. Sci Total Environ 793:148664

    Article  CAS  Google Scholar 

  • Wang WS, Mauleon R, Hu ZQ, Chebotarov D, Leung H (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557:7703

    Article  Google Scholar 

  • Watts DB, Torbert HA, Feng Y, Prior SA (2010) Soil microbial community dynamics as influenced by composted dairy manure, soil properties, and landscape position. Soil Sci 175:474–486

    Article  CAS  Google Scholar 

  • Wei M, Hu GQ, Wang H, Bai E, Lou YH, Zhang A, Zhuge YP (2017) 35 years of manure and chemical fertilizer application alters soil microbial community composition in a fluvo-aquic soil in Northern China. Eur J Soil Biol 82:27–34

    Article  Google Scholar 

  • Wei M, Zhang AJ, Tang ZH, Zhao P, Pan H, Wang H, Yang QH, Lou YH, Zhuge YP (2020) Active carbon pool-size is enhanced by long-term manure application. Plant Soil Environ 66:647–662

    Article  Google Scholar 

  • Weiss S, Treuren WV, Lozupone C, Faust K, Friedman J, Deng Y, Xia LC, Xu Z, Ursell L, Alm EJ (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J 10:1669–1681

    Article  CAS  Google Scholar 

  • Wen YL, Liu WJ, Deng WB, He XH, Yu GH (2019) Impact of agricultural fertilization practices on organo-mineral associations in four long-term field experiments. Implications for soil C sequestration. Sci Total Environ 651:591–600

    Article  CAS  Google Scholar 

  • Wickham H, Chang W, Wickham MH (2016) Package ‘ggplot2’:create elegant data visualisations using the grammar of graphics. Version 2:1–189

    Google Scholar 

  • Yang W, Yang Z, Guan Y, Zhai C, Shi DY (2020) Dose-dependent effect of compost amendment on soil bacterial community composition and co-occurrence network patterns in soybean agroecosystem. Arch Agron Soil Sci 66:1027–1041

    Article  CAS  Google Scholar 

  • Zhang H, Ullah F, Ahmad R (2022) Response of soil Proteobacteria to biochar amendment in sustainable agriculture-a mini review. Plant Soil Environ 1:16–30

    Article  Google Scholar 

  • Zhang X, Zhang R, Gao J, Wang X, Fan F, Ma X, Deng Y (2017) Thirty-one years of rice-rice-green manure rotations shape the rhizosphere microbial community and enrich beneficial bacteria. Soil Biol Biochem 104:208–217

  • Zhang XY, Li Y, Ouyang D, Lei JJ, Tan QL, Xie LL, Li ZQ, Liu T, Xiao YM, Farooq TH (2021a) Systematical review of interactions between microplastics and microorganisms in the soil environment. J Hazard Mater 418:126288

    Article  CAS  Google Scholar 

  • Zhang XX, Gao JS, Cao YH, Ma XT, He JZ (2013) Long-term rice and green manure rotation alters the endophytic bacterial communities of the rice root. Microb Ecol 66:917–926

    Article  Google Scholar 

  • Zhang ZM, Yan J, Han XZ, Zou WX, Chen X, Lu XC, Feng YT (2021b) Labile organic carbon fractions drive soil microbial communities after long-term fertilization. Glob Ecol Conserv 32:e01867

    Article  Google Scholar 

  • Zhou YP, Bastida F, Zhou B, Sun YF, Gu T, Li SQ (2020) Soil fertility and crop production are fostered by micro-nano bubble irrigation with associated changes in soil bacterial community. Soil Biol Biochem 141:107663

    Article  CAS  Google Scholar 

  • Ziska LH, Blumenthal DM, Runion GB, Hunt ER, Diaz-Soltero H (2011) Invasive species and climate change: an agronomic perspective. Clim Change 105:13–42

    Article  Google Scholar 

Download references

Acknowledgements

This work was jointly supported by grants from the National Natural Science Foundation of China (grant no. 42207367), the Basic Public Welfare Research Project of Zhejiang Province (no. LGN20C150003), and the China Postdoctoral Science Foundation (funded project no. 2022M711655).

Author information

Authors and Affiliations

  1. School of Life Science, Shaoxing University, Huancheng West Road 508, Shaoxing, 312000, People’s Republic of China

    Xiran Zhao, Jun Li, Xin Hu, Baowei Hu, Guixin Chu & Rui Tao

Authors
  1. Xiran Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Baowei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guixin Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rui Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rui Tao.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Yuan Ge

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 513 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, X., Li, J., Hu, X. et al. Three decades of organic manure and chemical fertilizers co-application enhanced rice productivity through increasing the diversity and key network module of soil bacterial community. J Soils Sediments 23, 2175–2188 (2023). https://doi.org/10.1007/s11368-023-03477-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-023-03477-z

Keywords

Search

Navigation