Predicting the structure of soil communities from plant community taxonomy, phylogeny, and traits

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There are numerous ways in which plants can influence the composition of soil communities. However, it remains unclear whether information on plant community attributes, including taxonomic, phylogenetic, or trait-based composition, can be used to predict the structure of soil communities. We tested, in both monocultures and field-grown mixed temperate grassland communities, whether plant attributes predict soil communities including taxonomic groups from across the tree of life (fungi, bacteria, protists, and metazoa). The composition of all soil community groups was affected by plant species identity, both in monocultures and in mixed communities. Moreover, plant community composition predicted additional variation in soil community composition beyond what could be predicted from soil abiotic characteristics. In addition, analysis of the field aboveground plant community composition and the composition of plant roots suggests that plant community attributes are better predictors of soil communities than root distributions. However, neither plant phylogeny nor plant traits were strong predictors of soil communities in either experiment. Our results demonstrate that grassland plant species form specific associations with soil community members and that information on plant species distributions can improve predictions of soil community composition. These results indicate that specific associations between plant species and complex soil communities are key determinants of biodiversity patterns in grassland soils.

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  1. 1.

    Bates ST, Clemente JC, Flores GE, Walters WA, Parfrey LW, Knight R, et al. Global biogeography of highly diverse protistan communities in soil. ISME J. 2013;7:652–9.

  2. 2.

    Fierer N, Strickland MS, Liptzin D, Bradford Ma, Cleveland CC. Global patterns in belowground communities. Ecol Lett. 2009;12:1238–49.

  3. 3.

    Kaiser K, Wemheuer B, Korolkow V, Wemheuer F, Nacke H, Schöning I, et al. Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests. Sci Rep. 2016;6:33696.

  4. 4.

    Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R. et al. Global diversity and geography of soil fungi. Science. 2014;346:1256688.

  5. 5.

    Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, et al. Plant-soil feedbacks: the past, the present and future challenges. J Ecol. 2013;101:265–76.

  6. 6.

    Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–33.

  7. 7.

    Bardgett RD, Wardle DA. Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. New York, NY, USA: Oxford University Press Oxford; 2010.

  8. 8.

    van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature. 1998;396:69–72.

  9. 9.

    Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, et al. Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol. 2014;203:233–44.

  10. 10.

    Singh BK, Millard P, Whiteley AS, Murrell JC. Unravelling rhizosphere–microbial interactions: opportunities and limitations. Trends Microbiol. 2004;12:386–93.

  11. 11.

    Berg G, Smalla K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol. 2009;68:1–13.

  12. 12.

    Grayston SJ, Wang S, Campbell CD, Edwards AC. Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem. 1998;30:369–78.

  13. 13.

    Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol. 1999;13:650–60.

  14. 14.

    Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem. 2001;33:533–51.

  15. 15.

    de Vries FT, Manning P, Tallowin JRB, Mortimer SR, Pilgrim ES, Harrison KA, et al. Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecol Lett. 2012;15:1230–9.

  16. 16.

    Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, et al. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett. 2015;18:85–95.

  17. 17.

    Lekberg Y, Waller LP. What drives differences in arbuscular mycorrhizal fungal communities among plant species? Fungal Ecol. 2006;24:135–138.

  18. 18.

    Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol. 2009;84:11–18.

  19. 19.

    Bezemer TM, Fountain MT, Barea JM, Christensen S, Dekker SC, Duyts H, et al. Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects. Ecology. 2010;91:3027–36.

  20. 20.

    St. John MG, Wall DH, Behan-Pelletier VM. Does plant species co-occurrence influence soil mite diversity? Ecology. 2006;87:625–33.

  21. 21.

    Gibbons SM, Lekberg Y, Mummey DL, Sangwan N, Ramsey PW, Gilbert JA. Invasive plants rapidly reshape soil properties in a grassland ecosystem. mSystems. 2017;2:e00178–16.

  22. 22.

    Hawkes CV, Wren IF, Herman DJ, Firestone MK. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett. 2005;8:976–85.

  23. 23.

    Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, et al. Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J Ecol. 2006;94:893–904.

  24. 24.

    Carey CJ, Michael Beman J, Eviner VT, Malmstrom CM, Hart SC. Soil microbial community structure is unaltered by plant invasion, vegetation clipping, and nitrogen fertilization in experimental semi-arid grasslands. Front Microbiol. 2015; 6.

  25. 25.

    Porazinska DL, Bardgett RD, Blaauw MB, Hunt HW, Parsons AN, Seastedt TR, et al. Relationships at the aboveground-belowground interface: plants, soil biota, and soil processes. Ecol Monogr. 2003;73:377–95.

  26. 26.

    Tedersoo L, Bahram M, Cajthaml T, Põlme S, Hiiesalu I, Anslan S et al. Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J. 2016;10:346–362.

  27. 27.

    Barberán A, Mcguire KL, Wolf JA, Jones FA, Wright SJ, Turner BL, et al. Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest. Ecol Lett. 2015;18:1397–405.

  28. 28.

    De Deyn GB, Van Der Putten WH. Linking aboveground and belowground diversity. Trends Ecol Evol. 2005;20:625–33.

  29. 29.

    Ben-Hur E, Fragman-Sapir O, Hadas R, Singer A, Kadmon R. Functional trade-offs increase species diversity in experimental plant communities. Ecol Lett. 2012;15:1276–82.

  30. 30.

    Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJB. Trait-based tests of coexistence mechanisms. Ecol Lett. 2013;16:1294–306.

  31. 31.

    Cantarel AAM, Pommier T, Desclos-Theveniau M, Diquélou S, Dumont M, Grassein F, et al. Using plant traits to explain plant–microbe relationships involved in nitrogen acquisition. Ecology. 2015;96:788–99.

  32. 32.

    Grigulis K, Lavorel S, Krainer U, Legay N, Baxendale C, Dumont M, et al. Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J Ecol. 2013;101:47–57.

  33. 33.

    Legay N, Lavorel S, Baxendale C, Krainer U, Bahn M, Binet M-N, et al. Influence of plant traits, soil microbial properties, and abiotic parameters on nitrogen turnover of grassland ecosystems. Ecosphere. 2016;7:1–17.

  34. 34.

    Moreau D, Pivato B, Bru D, Busset H, Deau F, Faivre C, et al. Plant traits related to nitrogen uptake influence plant-microbe competition. Ecology. 2015;96:2300–10.

  35. 35.

    Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, et al. Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol. 2010;98:1074–83.

  36. 36.

    Legay N, Baxendale C, Grigulis K, Krainer U, Kastl E, Schloter M, et al. Contribution of above- and below-ground plant traits to the structure and function of grassland soil microbial communities. Ann Bot. 2014;114:1011–21.

  37. 37.

    Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI. Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol Ecol. 2016;92.

  38. 38.

    Bardgett RD, Mommer L, De Vries FT. Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol. 2014;29:692–9.

  39. 39.

    De Deyn GB, Shiel RS, Ostle NJ, Mcnamara NP, Oakley S, Young I, et al. Additional carbon sequestration benefits of grassland diversity restoration. J Appl Ecol. 2011;48:600–8.

  40. 40.

    Rodwell JS. (1992). British plant communities. Volume 3. Grassland and montane communities. 3rd ed. Cambridge University Press: Cambridge, U.K.

  41. 41.

    Smith RS, Shiel RS, Bardgett RD, Millward D, Corkhill P, Rolph G, et al. Soil microbial community, fertility, vegetation and diversity as targets in the restoration management of a meadow grassland. J Appl Ecol. 2003;40:51–64.

  42. 42.

    Ramirez KS, Leff JW, Barberán A, Bates ST, Betley J, Crowther TW, 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 Biol Sci. 2014;281:1–9.

  43. 43.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high resolution sample inference from amplicon data. Nat Methods. 2016;13:581–3.

  44. 44.

    Abarenkov K, Henrik Nilsson R, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, et al. The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol. 2010;186:281–5.

  45. 45.

    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. 2012;6:610–8.

  46. 46.

    Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner 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. 2013;41:597–604.

  47. 47.

    Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108:1028–46.

  48. 48.

    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. 2015;20:241–8.

  49. 49.

    Kartzinel TR, Chen Pa, Coverdale TC, Erickson DL, Kress WJ, Kuzmina ML, et al. DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc Natl Acad Sci USA. 2015;112:8019–24.

  50. 50.

    Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, et al. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot. 2003;51:335–80.

  51. 51.

    Bardgett RD, Streeter TC, Bol R. Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology. 2003;84:1277–87.

  52. 52.

    R Core Team R: A language and environment for statistical computing 2016. R Foundation for Statistical Computing: Vienna, Austria.

  53. 53.

    Dufrêne M, Legendre P. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol Monogr. 1997;67:345–66.

  54. 54.

    Durka W, Michalski SG. Daphne: a dated phylogeny of a large European flora for phylogenetically informed ecological analyses. Ecology. 2012;93:2297.

  55. 55.

    Blomberg SP, Garland T, Ives AR. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution. 2003;57:717–45.

  56. 56.

    Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011;5:169–72.

  57. 57.

    Leff JW, Jones SE, Prober SM, Barberan 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;112:10967–72.

  58. 58.

    Wu T, Ayres E, Bardgett RD, Wall DH, Garey JR. Molecular study of worldwide distribution and diversity of soil animals. Proc Natl Acad Sci USA. 2011;108:17720–5.

  59. 59.

    Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR. Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology. 2012;93:1867–79.

  60. 60.

    Peay KG, Baraloto C, Fine PVA. Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME J. 2013;7:1852–61.

  61. 61.

    Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY. Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett. 2014;17:1613–21.

  62. 62.

    Mehrabi Z, Tuck SL. Relatedness is a poor predictor of negative plant-soil feedbacks. New Phytol. 2015;205:1071–5.

  63. 63.

    Lavorel S, Garnier E. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol. 2002;16:545–56.

  64. 64.

    Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S et al. Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol. 2016.

  65. 65.

    Barberán A, Dunn RR, Reich BJ, Pacifici K, Laber EB, Menninger HL, et al. The ecology of microscopic life in household dust. Proc R Soc B. 2015;282:1–9.

  66. 66.

    Haichar FEZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, et al. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2008;2:1221–30.

  67. 67.

    Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol 2016;2.

  68. 68.

    Yoccoz NG, Bråthen KA, Gielly L, Haile J, Edwards ME, Goslar T, et al. DNA from soil mirrors plant taxonomic and growth form diversity. Mol Ecol. 2012;21:3647–55.

  69. 69.

    Hiiesalu I, Öpik M, Metsis M, Lilje L, Davison J, Vasar M, et al. Plant species richness belowground: higher richness and new patterns revealed by next-generation sequencing. Mol Ecol. 2012;21:2004–16.

  70. 70.

    Harrison KA, Bardgett RD. Influence of plant species and soil conditions on plant-soil feedback in mixed grassland communities. J Ecol. 2010;98:384–95.

  71. 71.

    Laliberté E. Below-ground frontiers in trait-based plant ecology. New Phytol. 2017;213:1597–603.

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We thank Emily Morgan for her assistance with the microbial community analyses, Colin Newlands of Natural England for permission to use the field sites, and Marina Semchenko for comments on a previous version of this manuscript. We also thank all who helped establish the field experimental site and collect and process the plant and soil samples: Aurore Kaisermann, Debora Ashworth, Angela Straathof, Imelda Uwase, Marina Semchenko, Maatren Schrama, Melanie Edgar, Mark Bradford, Mike Whitfield, Rachel Marshall, and Andrew Cole.


This research was supported by a grant from the UK Biotechnology and Biological Sciences Research Council (BBSRC) (Grant BB/I009000/2), initiated and led by RDB, a BBSRC International Exchange Grant (BB/L026406/1) between RDB and NF, and a grant from the U.S. National Science Foundation (NSF) (DEB 1542653) awarded to NF.

Author information


  1. Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, 80309, USA

    • Jonathan W. Leff
    •  & Noah Fierer
  2. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    • Jonathan W. Leff
    •  & Noah Fierer
  3. School of Earth and Environmental Sciences, Michael Smith Building, The University of Manchester, Oxford Road, Manchester, M13 9PT, UK

    • Richard D. Bardgett
    • , Anna Wilkinson
    • , William J. Pritchard
    • , Jonathan R. De Long
    •  & David Johnson
  4. School of Geosciences, Grant Institute, The King’s Buildings, James Hutton Road, Edinburgh, EH9 3FE, UK

    • Benjamin G. Jackson
  5. Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, LA1 4AP, UK

    • Simon Oakley
    •  & Kelly E. Mason
  6. Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK

    • Nicholas J. Ostle
  7. The Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus Buildings, Midlothian, EH25 9RG, UK

    • Elizabeth M. Baggs


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Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Noah Fierer.

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