Abstract

The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential ‘indicator’ taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.

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Acknowledgements

We thank all the people who contributed data and input to this study. This study was conducted at a workshop (May 2015, Manchester, UK) funded by the British Ecological Society’s special interest group Plants-Soils-Ecosystems and organized by F.T.d.V. and K.S.R. This study and participants were funded in part by ERC Advanced Grant 26055290 (K.S.R., and W.H.v.d.P.); BBSRC David Phillips Fellowship (BB/L02456X/1) (F.T.d.V.); ERC Grant Agreements 242658 (BIOCOM) and 647038 (BIODESERT) (F.T.M.); the European Regional Development Fund (Centre of Excellence EcolChange) (J.D.); Yorkshire Agricultural Society, Nafferton Ecological Farming Group, and the Northumbria University Research Development Fund (C.H.O.); BBSRC Training Grant (BB/K501943/1) (C.H.); Wallenberg Academy Fellowship (KAW 2012.0152), Formas (214-2011-788) and Vetenskapsrådet (612-2011-5444) (E.D.); the Glastir Monitoring & Evaluation Programme (contract reference: C147/2010/11) and the full support of the GMEP team on the Glastir project (D.L.J., S.C., and D.A.R.). Computing was facilitated by the University of Manchester Condor pool and the CLIMB infrastructure (http://www.climb.ac.uk).

Author information

Author notes

  1. Kelly S. Ramirez and Christopher G. Knight contributed equally to this work.

Affiliations

  1. Netherlands Institute of Ecology, Wageningen, The Netherlands

    • Kelly S. Ramirez
    • , Mattias de Hollander
    • , Thomas W. Crowther
    •  & Wim H. van der Putten
  2. Faculty of Science and Engineering, University of Manchester, Manchester, UK

    • Christopher G. Knight
    • , Angela L. Straathof
    •  & Franciska T. de Vries
  3. School of Science and the Environment, Manchester Metropolitan University, Manchester, UK

    • Francis Q. Brearley
    • , David R. Elliott
    • , Graeme Fox
    •  & Jennifer Rowntree
  4. Evolution and Genomic Sciences, School of Biological Sciences, University of Manchester, Manchester, UK

    • Bede Constantinides
  5. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK

    • Anne Cotton
  6. Environment Centre Wales, College of Natural Sciences, Bangor University, Bangor, UK

    • Si Creer
    •  & David L. Jones
  7. Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland

    • Thomas W. Crowther
  8. Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia

    • John Davison
  9. Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, USA

    • Manuel Delgado-Baquerizo
  10. Climate Impacts Research Centre, Department of Ecology and Environmental Science, Umeå University, Abisko, Sweden

    • Ellen Dorrepaal
    • , Eveline J. Krab
    •  & Sylvain Monteux
  11. Environmental Sustainability Research Centre, University of Derby, Derby, UK

    • David R. Elliott
  12. Centre for Ecology and Hydrology, Wallingford, UK

    • Robert I. Griffiths
  13. School of Life Sciences, University of Warwick, Coventry, UK

    • Chris Hale
  14. Division of Agroecology and Environment, Agroscope, Zürich, Switzerland

    • Kyle Hartman
    • , Klaus Schlaeppi
    •  & Marcel G. A. van der Heijden
  15. Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK

    • Ashley Houlden
    •  & Ian S. Roberts
  16. Departamento de Biología y Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Móstoles, Spain

    • Fernando T. Maestre
  17. Department of Biology, Institute of Ecology and Evolution, University of Oregon, Eugene, OR, USA

    • Krista L. McGuire
  18. School of Science and Engineering, Teesside University, Middlesbrough, UK

    • Caroline H. Orr
  19. Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands

    • Wim H. van der Putten
  20. Centre for Ecology and Hydrology, Bangor, UK

    • David A. Robinson
  21. Department of Biology, Duke University, Durham, NC, USA

    • Jennifer D. Rocca
  22. Natural England, Exeter, UK

    • Matthew Shepherd
  23. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia

    • Brajesh K. Singh
  24. Department of Biology, Boston University, Boston, MA, USA

    • Jennifer M. Bhatnagar
  25. Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, UK

    • Cécile Thion
  26. Institute for Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, Switzerland

    • Marcel G. A. van der Heijden
  27. Plant–Microbe Interactions, Institute of Environmental Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands

    • Marcel G. A. van der Heijden

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Contributions

The idea for this study was conceived by F.T.d.V. and K.S.R. The data sets were compiled by C.G.K., R.G., J.D., A.H., B.C., G.F., A.L.S., and J.R. Metadata were compiled by J.D. and J.R. Raw sequence analysis was conducted by M.d.H. Primer bias analysis was conducted by A.C. Random Forest analyses and figures were conducted by C.G.K. The manuscript was written by K.S.R., C.G.K., and F.T.d.V., with contributions from all co-authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Kelly S. Ramirez.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Tables 2 and 3 and Supplementary Figures 1–10.

  2. Life Sciences Reporting Summary

  3. Figure Generation Data

    Supplementary Table 4: Data used to generate figures.

  4. Figure Generation Code

    R code use to generate figures.

  5. Supplementary Table 1

    Summary of all datasets used.

  6. Supplementary Table 5

    Name-matched data.

  7. Supplementary Table 6

    Sequence-matched data.