Abstract
Cropping systems have fertilized soils for decades with undetermined consequences for the productivity and functioning of terrestrial ecosystems. One of the critical unknowns is the role of soil biodiversity in controlling crop production after decades of fertilization. This knowledge gap limits our capacity to assess how changes in soil biodiversity could alter crop production and soil health in changing environments. Here, we used multitrophic ecological networks to investigate the importance of soil biodiversity, in particular, the biodiversity of key-stone taxa in controlling soil functioning and wheat production in a 35-year field fertilization experiment. We found strong and positive associations between soil functional genes, crop production and the biodiversity of key-stone phylotypes; soils supporting a larger number of key-stone nematode, bacteria and fungi phylotypes yielded the highest wheat production. These key-stone phylotypes were also positively associated with plant growth (phototrophic bacteria, nitrogen fixers) and multiple functional genes related to nutrient cycling. The retrieved information on the genomes clustered with key-stone bacterial phylotypes indicated that the key-stone taxa had higher gene copies of oxidoreductases (participating most biogeochemical cycles of ecosystems and linking to microbial energetics) and 71 essential functional genes associated with carbon, nitrogen, phosphorus, and sulfur cycling. Altogether, our work highlights the fundamental role of the biodiversity of key-stone phylotypes in maintaining soil functioning and crop production after several decades of fertilization, and provides a list of key-stone phylotypes linking to crop production and soil nutrient cycling, which could give science-based guidance for sustainable food production.
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References
Delgado-Baquerizo M, Reich PB, Trivedi C, Eldridge DJ, Abades S, Alfaro FD, et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol. 2020;4:210–20.
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. 2016;7:10541.
Shah F, Wu W. Soil and crop management strategies to ensure higher crop productivity within sustainable environments. Sustainability. 2019;11:1485.
Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci USA. 2015;112:10967.
Sun R, Zhang X-X, Guo X, Wang D, Chu H. 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. 2015;88:9–18.
Mougi A, Kondoh M. Diversity of interaction types and ecological community stability. Science. 2012;337:349–51.
Kumar A, Patel JS, Meena VS. Rhizospheric microbes for sustainable agriculture: an overview. In: Meena VS, editor. Role of rhizospheric microbes in soil: volume 1: stress management and agricultural sustainability. Singapore: Springer Singapore; 2018. p. 1–31.
Yeates GW, Bongers T. Nematode diversity in agroecosystems. In: Paoletti MG, editor. Invertebrate biodiversity as bioindicators of sustainable landscapes. Amsterdam: Elsevier; 1999. p. 113–35.
Chaffron S, Rehrauer H, Pernthaler J, von Mering C. A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res. 2010;20:947–59.
Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.
Cai G, Chen D, Ding H, Pacholski A, Fan X, Zhu Z. Nitrogen losses from fertilizers applied to maize, wheat and rice in the North China Plain. Nutr Cycl Agroecosys. 2002;63:187–95.
Fan K, Delgado-Baquerizo M, Guo X, Wang D, Wu Y, Zhu M, et al. Suppressed N fixation and diazotrophs after four decades of fertilization. Microbiome. 2019;7:143.
Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci USA. 2008;105:10583–8.
Bokulich NA, Mills DA. Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol. 2013;79:2519–26.
Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V. Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol. 2010;12:2165–79.
Porazinska D, Giblin-Davis, Robin M, Faller LF, William K, Natsumi M, et al. Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Mol Ecol Resour. 2009;9:1439–50.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2011;6:610.
Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. N. Phytol. 2005;166:1063–8.
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, et al. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). N Phytol. 2010;188:223–41.
Quast C, Pruesse E, Gerken J, Peplies J, Yarza P, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–D6.
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 2016;20:241–8.
Dean R, Kan JALV, Pretorius ZA, Hammond‐Kosack KE, Pietro AD, Spanu PD, et al. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13:804.
Wang F-H, Qiao M, Su J-Q, Chen Z, Zhou X, Zhu Y-G. High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ Sci Technol. 2014;48:9079–85.
Zheng B, Zhu Y, Sardans J, Peñuelas J, Su J. QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Sci China Life Sci. 2018;61:1451–62.
Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 2001;29:e45–e45.
Langfelder P, Horvath S. Fast R functions for robust correlations and hierarchical clustering. J Stat Softw. 2012;46:11.
Benjamini Y, Krieger AM, Yekutieli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika. 2006;93:491–507.
Hines J, van der Putten WH, De Deyn GB, Wagg C, Voigt W, Mulder C, et al. Chapter four-Towards an integration of biodiversity–ecosystem functioning and food web theory to evaluate relationships between multiple ecosystem services. Adv Ecol Res. 2015;53:161–99.
Menezes AB, Prendergast-Miller MT, Richardson AE, Toscas P, Farrell M, Macdonald LM, et al. Network analysis reveals that bacteria and fungi form modules that correlate independently with soil parameters. Environ Microbiol. 2015;17:2677–89.
Heleno R, Devoto M, Pocock M. Connectance of species interaction networks and conservation value: Is it any good to be well connected? Ecol Indic. 2012;14:7–10.
Ramírez-Flandes S, González B, Ulloa O. Redox traits characterize the organization of global microbial communities. Proc Natl Acad Sci USA. 2019;116:3630.
Pérez Castro S, Cleland EE, Wagner R, Sawad RA, Lipson DA. Soil microbial responses to drought and exotic plants shift carbon metabolism. ISME J. 2019;13:1776–87.
Zhang C, Song Z, Zhuang D, Wang J, Xie S, Liu G. Urea fertilization decreases soil bacterial diversity, but improves microbial biomass, respiration, and N-cycling potential in a semiarid grassland. Biol Fert Soils. 2019;55:229–42.
Fraser TD, Lynch DH, Bent E, Entz MH, Dunfield KE. Soil bacterial phoD gene abundance and expression in response to applied phosphorus and long-term management. Soil Biol Biochem. 2015;88:137–47.
García-Palacios P, Shaw EA, Wall DH, Hättenschwiler S. Temporal dynamics of biotic and abiotic drivers of litter decomposition. Ecol Lett. 2016;19:554–63.
Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR, et al. Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome. 2013;1:22.
Lu J, Yang F, Wang S, Ma H, Liang J, Chen Y. Co-existence of rhizobia and diverse non-rhizobial bacteria in the rhizosphere and nodules of dalbergia odorifera seedlings inoculated with Bradyrhizobium elkanii, Rhizobium multihospitium–like and Burkholderia pyrrocinia–like strains. Front Microbiol. 2017;8:2255.
Haack FS, Poehlein A, Kröger C, Voigt CA, Piepenbring M, Bode HB, et al. Molecular keys to the janthinobacterium and duganella spp. interaction with the plant pathogen Fusarium graminearum. Front Microbiol. 2016;7:1668.
Clay K, Leuchtmann A. Infection of woodland grasses by fungal endophytes. Mycologia. 1989;81:805–11.
Huang X, Liu L, Wen T, Zhang J, Wang F, Cai Z. Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biotechnol. 2016;100:5581–93.
Palleroni NJ. Pseudomonas. In: M.E. Trujillo, S. Dedysh, P. DeVos, B. Hedlund, P. Kämpfer, F.A. Rainey and W.B. Whitman, editors. Bergeyʼs Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, Inc. in association with Bergey’s Manual Trust; 2015. p. 1–105.
Wei Z, Yang T, Friman V-P, Xu Y, Shen Q, Jousset A. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun. 2015;6:8413.
Mao Y, Li X, Smyth EM, Yannarell AC, Mackie RI. Enrichment of specific bacterial and eukaryotic microbes in the rhizosphere of switchgrass (Panicum virgatum L.) through root exudates. Environ Microbiol Rep. 2014;6:293–306.
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, et al. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev. 2016;80:1.
Agnolucci M, Battini F, Cristani C, Giovannetti M. Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biol Fert Soils. 2015;51:379–89.
Levy A, Merritt AJ, Mayo MJ, Chang BJ, Abbott LK, Inglis TJJ. Association between Burkholderia species and arbuscular mycorrhizal fungus spores in soil. Soil Biol Biochem. 2009;41:1757–9.
Li X, Rui J, Xiong J, Li J, He Z, Zhou J, et al. Functional potential of soil microbial communities in the maize rhizosphere. PLoS ONE. 2014;9:e112609.
Ragot SA, Kertesz MA, Mészáros É, Frossard E, Bünemann EK. Soil phoD and phoX alkaline phosphatase gene diversity responds to multiple environmental factors. FEMS Microbiol Ecol. 2016;93:fiw212.
Gianfreda L. Enzymes of importance to rhizosphere processes. J Soil Sc Plant Nutr. 2015;15:283–306.
Su J-Q, Ding L-J, Xue K, Yao H-Y, Quensen J, Bai S-J, et al. Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol. 2015;24:136–50.
Ratliff TJ, Fisk MC. Phosphatase activity is related to N availability but not P availability across hardwood forests in the northeastern United States. Soil Biol Biochem. 2016;94:61–9.
Acknowledgements
We thank Ruibo Sun, Jianqiang Su, Xinyuan Zhou, Zhibin Guo, Keke Hua, Yingying Ni, Yuying Ma, Hongfei Wang, Liang Cheng, Yu Shi, Teng Yang, and Yuntao Li for their assistance in field management, soil sampling, and laboratory work. This work was funded by the National Natural Science Foundation of China (31870480), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15010101), and the China Biodiversity Observation Networks (Sino BON). MD-B is supported by a Ramón y Cajal grant from the Spanish Government (agreement no. RYC2018-025483-I).
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Fan, K., Delgado-Baquerizo, M., Guo, X. et al. Biodiversity of key-stone phylotypes determines crop production in a 4-decade fertilization experiment. ISME J 15, 550–561 (2021). https://doi.org/10.1038/s41396-020-00796-8
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DOI: https://doi.org/10.1038/s41396-020-00796-8
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