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Understanding how microbiomes influence the systems they inhabit

Nature Microbiology volume 3, pages 977–982 (2018)Cite this article

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Abstract

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.

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Fig. 1: Diagram of microbial–ecosystem linkages.
Fig. 2: A conceptual map of the intersection between microbial (vertical) and ecosystem (horizontal) ecology.

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Acknowledgements

This work is a product of the Next Generation of Ecosystem Indicators Working Group, supported by the USGS John Wesley Powell Center for Synthesis and Analysis. Development of this manuscript was supported by NSF DEB IOS #1456959, awarded to E.K.H., and was prepared in part by E.K.H. as writer in residence at the Wolverine Farm Publick House and Press. C. Pepe-Ranney and A. Peralta provided valuable feedback on previous versions of this manuscript. This paper is dedicated to D. Nemergut, an integral part of our working group who passed away during the preparation of this manuscript.

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Authors and Affiliations

  1. Colorado State University, Fort Collins, CO, USA

    Ed K. Hall, Claudia M. Boot, Jennifer D. Rocca & Matthew D. Wallenstein

  2. Duke University, Durham, NC, USA

    Emily S. Bernhardt, Raven L. Bier, Diana Nemergut & Jennifer D. Rocca

  3. Stroud Water Center, Avondale, PA, USA

    Raven L. Bier

  4. Yale University, School of Forestry and Environmental Studies, New Haven, CT, USA

    Mark A. Bradford

  5. University of Minnesota, Saint Paul, MN, USA

    James B. Cotner

  6. Université du Québec à Montréal, Montréal, Quebec, Canada

    Paul A. del Giorgio

  7. Michigan State University, Hickory Corners, MI, USA

    Sarah E. Evans

  8. Institute of Arctic and Alpine Research, University of Colorado at Boulder, Boulder, CO, USA

    Emily B. Graham

  9. Pacific Northwest National Laboratory, Richland, WA, USA

    Emily B. Graham

  10. University of Notre Dame, South Bend, IN, USA

    Stuart E. Jones

  11. Indiana University, Bloomington, IN, USA

    Jay T. Lennon & Kenneth J. Locey

  12. Diné College, School of Science, Engineering, Technology and Math Tsaile, AZ, USA

    Kenneth J. Locey

  13. Brown University, Providence, RI, USA

    Brooke B. Osborne

  14. University of California, Santa Barbara, Santa Barbara, CA, USA

    Joshua P. Schimel

  15. US Geological Survey, Menlo Park, CA, USA

    Mark P. Waldrop

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All listed authors have contributed to the conceptualization, writing and preparation of the manuscript.

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Correspondence to Ed K. Hall.

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Hall, E.K., Bernhardt, E.S., Bier, R.L. et al. Understanding how microbiomes influence the systems they inhabit. Nat Microbiol 3, 977–982 (2018). https://doi.org/10.1038/s41564-018-0201-z

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