The role of soil biodiversity in regulating multiple ecosystem functions is poorly understood, limiting our ability to predict how soil biodiversity loss might affect human wellbeing and ecosystem sustainability. Here, combining a global observational study with an experimental microcosm study, we provide evidence that soil biodiversity (bacteria, fungi, protists and invertebrates) is significantly and positively associated with multiple ecosystem functions. These functions include nutrient cycling, decomposition, plant production, and reduced potential for pathogenicity and belowground biological warfare. Our findings also reveal the context dependency of such relationships and the importance of the connectedness, biodiversity and nature of the globally distributed dominant phylotypes within the soil network in maintaining multiple functions. Moreover, our results suggest that the positive association between plant diversity and multifunctionality across biomes is indirectly driven by soil biodiversity. Together, our results provide insights into the importance of soil biodiversity for maintaining soil functionality locally and across biomes, as well as providing strong support for the inclusion of soil biodiversity in conservation and management programmes.
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Soil biodiversity and functional data from the global field survey and the microcosm experiment are publicly available in Figshare51.
Holzman, D. C. Accounting for nature’s benefits: the dollar value of ecosystem services. Environ. Health Perspect. 120, a152–a157 (2012).
Wagg, C. et al. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl Acad. Sci. USA 111, 5266–70 (2014).
Van Elsas, J. D. et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl Acad. Sci. USA 109, 1159–1164 (2012).
Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–11 (2014).
Wall, D. H., Nielsen, U. N. & Six, J. Soil biodiversity and human health. Nature 528, 69–76 (2015).
van den Hoogen, J. et al. Soil nematode abundance and functional group composition at a global scale. Nature 572, 194–198 (2019).
Troudet, J. et al. Taxonomic bias in biodiversity data and societal preferences. Sci. Rep. 7, 9132 (2017).
Allan, E. et al. Interannual variation in land-use intensity enhances grassland multidiversity. Proc. Natl Acad. Sci. USA 111, 308–313 (2014).
Bradford, M. A. Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. Proc. Natl Acad. Sci. USA 111, 14478–14483 (2014).
Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016).
Soliveres, S. et al. Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature 536, 456–9 (2016).
Hättenschwiler, S. & Gasser, P. Soil animals alter plant litter diversity effects on decomposition. Proc. Natl Acad. Sci. USA 102, 1519–24 (2005).
García-Palacios, P. et al. Climate and litter quality differently modulate the effects of soil fauna on litter decomposition across biomes. Ecol. Lett. 16, 1045–53 (2013).
Byrnes, J. E. et al. Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Meth. Ecol. Evol. 5, 111–124 (2014).
Geisen, S. The bacterial-fungal energy channel concept challenged by enormous functional versatility of soil protists. Soil Biol. Biochem. 102, 22–25 (2016).
Bonkowski, M. Protozoa and plant growth. New Phytol. 162, 617–631 (2004).
Menezes, A. B. et al. Network analysis reveals that bacteria and fungi form modules that correlate independently with soil parameters. Environ. Microbiol. 17, 2677–2689 (2015).
Barberán, A. et al. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 6, 343–351 (2012).
de Vries, F. T. et al. Soil bacterial networks are less stable under drought than fungal networks. Nat. Commun. 9, 3033 (2018).
Delgado-Baquerizo, M. et al. A global atlas of the dominant bacteria found in soil. Science 359, 320–325 (2018).
Guimerà, R. & Amaral, L. A. Functional cartography of complex metabolic networks. Nature 433, 895–900 (2005).
Jens, M. & Olesen, J. M. et al. The modularity of pollination networks. Proc. Natl Acad. Sci. USA 104, 19891–19896 (2007).
Bascompte, J. & Stouffer, D. B. The assembly and disassembly of ecological networks. Proc. R. Soc. B 364, 1781–1787 (2009).
Gotelli, N. J. & Colwell, R. K. in Biological Diversity: Frontiers in Measurement and Assessment (eds Magurran, A. E. & McGill, B. J.) 39–54 (Oxford Univ. Press, 2011).
Maestre, F. T. et al. Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218 (2012).
Manning, P. et al. Redefining ecosystem multifunctionality. Nat. Ecol. Evol. 2, 427–436 (2018).
Philippot, L. et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 7, 1609–19 (2013).
Delgado‐Baquerizo, M. et al. Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning. J. Ecol. 104, 936–946 (2016).
Banerjee S., Schlaeppi K. & van der Heijden, M. G. A. Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 16, 567–576 (2018).
Bahram, M., Hildebrand, F., Forslund, S. K., Anderson, J. L., Soudzilovskaia, N. A. & Bodegom, P. M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).
Kettler, T. A. et al. Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci. Soc.Am. J 65, 849–852 (2001).
Fierer, N. et al. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc. Natl Acad. Sci. USA 109, 21390–5 (2012).
Ramirez, K. S. et al. Biogeographic patterns in below-ground diversity in New York City’s Central Park are similar to those observed globally. Proc. R. Soc. B 281, 1795 (2014).
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460 (2010).
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
Guillou, L. et al. The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, 597–604 (2013).
Glassman S. I. & Martiny J. B. H. Broadscale ecological patterns are robust to use of exact sequence variants versus operational taxonomic units. mSphere 3, e00148-18 (2018).
Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fung. Ecol. 20, 241–248 (2016).
Delgado-Baquerizo, M. et al. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502, 672–676 (2013).
Bell, C. W. et al. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J. Vis. Exp. 81, e50961 (2013).
Campbell, C. D. et al. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl. Env. Microbiol. 69, 3593–3599 (2013).
Hu, H.-W. et al. Diversity of herbaceous plants and bacterial communities regulates soil resistome across forest biomes. Envir. Microbiol. 20, 3186–3200 (2018).
Bastida, F. et al. Phylogenetic and functional changes in the microbial community of long-term restored soils under semiarid climate. Soil Biol. Biochem. 65, 12–21 (2013).
Derrien, D. et al. Does the addition of labile substrate destabilise old soil organic matter? Soil Biol. Biochem. 76, 149–160 (2014).
Hopkins, F. M. et al. Increased belowground carbon inputs and warming promote loss of soil organic carbon through complementary microbial responses. Soil Biol. Biochem. 76, 57–69 (2014).
Kuzyakov, Y. Priming effects: interactions between living and dead organic matter. Soil Biol. Biochem. 42, 1363–1371 (2010).
Wolf, D. C. et al. Influence of sterilization methods on selected soil microbiological, physical, and chemical properties. J. Environ. Qual. 18, 39–44 (1989).
Lotrario, J. B. et al. Effects of sterilization methods on the physical characteristics of soil: implications for sorption isotherm analyses. Bull. Environ. Contam. Toxicol. 54, 668–675 (1995).
Csárdi, G. igraph, network analysis and visualization. R package version 1.2.2. R package (2018).
Watson, C. G. brainGraph, graph theory analysis of brain MRI data. R package version 2.2.0 (2018).
Delgado-Baquerizo, M. et al. Data from: Multiple elements of soil biodiversity drive ecosystem functions across biomes. Figshare https://doi.org/10.6084/m9.figshare.9976556 (2020).
We thank N. Fierer, M. Gebert, J. Henley, V. Ochoa, F. T. Maestre and B. Gozalo for their help with laboratory analyses; O. Sala, C. Siebe, C. Currier, M. A. Bowker, V. Parry, H. Lambers, P. Vitousek, V. M. Peña-Ramírez, L. Riedel, J. Larson, K. Waechter, W. Williams, S. Williams, B. Sulman, D. Buckner and B. Anacker for their help with soil sampling in Colorado, Hawaii, Iceland, New Mexico, Arizona, Mexico and Australia; the City of Boulder Open Space and Mountain Parks for allowing us to conduct these samplings; C. Cano-Díaz for her advice about R analyses; S. K. Travers for her help with mapping. This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 702057. M.D.-B. is supported by the Spanish Government under a Ramón y Cajal contract RYC2018-025483-I. This research is supported by the Australian Research Council projects (DP170104634; DP190103714). S.A. and F.D.A. are funded by FONDECYT 1170995, IAI-CRN 3005, PFB-23 (from CONICYT) and P05-002 (from Millennium Scientific Initiative). N.A.C. acknowledges support from Churchill College, University of Cambridge; and M.A.W. from the Wilderness State Park, Michigan for access to sample soil and conduct ecosystem survey. B.K.S. acknowledges a research award from the Humboldt Foundation. J.-Z.H. acknowledges support from the Australia Research Council (project DP170103628); and A.G. from the Spanish Ministry (project CGL2017-88124-R). F.B. thanks the Spanish Ministry and FEDER funds for the CICYT project AGL2017-85755-R, the CSIC project 201740I008 and funds from ‘Fundación Séneca’ from Murcia Province (19896/GERM/15). P.T. thanks K. Little for her help with laboratory analyses. S.C.R. was supported by the US Geological Survey Ecosystems Mission Area. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the US Government. S.N. was funded by the Austrian Science Fund (grant Y801-B16).
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Delgado-Baquerizo, M., Reich, P.B., Trivedi, C. et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol 4, 210–220 (2020). https://doi.org/10.1038/s41559-019-1084-y
BII-Implementation: The causes and consequences of plant biodiversity across scales in a rapidly changing world
Research Ideas and Outcomes (2021)
Daucus carota L. Seed Inoculation with a Consortium of Bacteria Improves Plant Growth, Soil Fertility Status and Microbial Community
Applied Sciences (2021)
Effect of Ionizing Radiation on the Bacterial and Fungal Endophytes of the Halophytic Plant Kalidium schrenkianum
Contrasting soil microbial abundance and diversity on and between pasture drill rows in the third growing season after sowing
Renewable Agriculture and Food Systems (2021)
Above- and belowground biodiversity drives soil multifunctionality along a long-term grassland restoration chronosequence
Science of The Total Environment (2021)