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Function and functional redundancy in microbial systems

Nature Ecology & Evolution volume 2, pages 936–943 (2018)Cite this article

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Abstract

Microbial communities often exhibit incredible taxonomic diversity, raising questions regarding the mechanisms enabling species coexistence and the role of this diversity in community functioning. On the one hand, many coexisting but taxonomically distinct microorganisms can encode the same energy-yielding metabolic functions, and this functional redundancy contrasts with the expectation that species should occupy distinct metabolic niches. On the other hand, the identity of taxa encoding each function can vary substantially across space or time with little effect on the function, and this taxonomic variability is frequently thought to result from ecological drift between equivalent organisms. Here, we synthesize the powerful paradigm emerging from these two patterns, connecting the roles of function, functional redundancy and taxonomy in microbial systems. We conclude that both patterns are unlikely to be the result of ecological drift, but are inevitable emergent properties of open microbial systems resulting mainly from biotic interactions and environmental and spatial processes.

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Fig. 1: Gene-centric structure of microbial communities can decouple from taxonomic composition.
Fig. 2: Phylogenetic conservatism varies between functions and between clades.
Fig. 3: Functional redundancy in methanogenic communities (schematic illustration).

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Acknowledgements

We thank M. Pennell, F. Doolittle, A. C. Martiny and I. Rubin for discussions and for participation at a workshop from which this Perspective emerged. We thank the Canadian Institute for Ecology and Evolution (CIEE) for financial support of all authors, by means of a Thematic Working Group grant on the ‘evolution of microbial metabolic and genomic diversity at multiple scales’. We thank the Biodiversity Research Centre and the Adapting Biosystems programme, University of British Columbia, for financial support, and K. Beall for logistical support. S.L. was supported by an NSERC grant and a postdoctoral fellowship from the Biodiversity Research Centre, UBC. J.A.H. was supported by the NSF Center for Dark Energy Biosphere Investigations (OCE-0939564).

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Authors and Affiliations

  1. Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    Stilianos Louca, Florent Mazel, Mary I. O’Connor, Diane S. Srivastava, Michael Doebeli & Laura Wegener Parfrey

  2. Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

    Stilianos Louca, Mary I. O’Connor, Diane S. Srivastava, Michael Doebeli & Laura Wegener Parfrey

  3. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

    Martin F. Polz

  4. Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada

    Florent Mazel & Laura Wegener Parfrey

  5. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    Florent Mazel

  6. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, USA

    Michaeline B. N. Albright

  7. Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Julie A. Huber

  8. Department of Environmental Systems Science, Eidgenössische Technische Hochschule Zürich, Zürich, Switzerland

    Martin Ackermann

  9. Department of Environmental Microbiology, Eawag, Dübendorf, Switzerland

    Martin Ackermann

  10. Ecosystem Services, Commercialization Platforms, and Entrepreneurship (ECOSCOPE) Training Program, University of British Columbia, Vancouver, British Columbia, Canada

    Aria S. Hahn & Sean A. Crowe

  11. Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada

    Sean A. Crowe

  12. Department of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada

    Sean A. Crowe

  13. Department of Mathematics, University of British Columbia, Vancouver, British Columbia, Canada

    Michael Doebeli

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S.L., L.W.P. and M.D. organized the workshop from which this Perspective emerged. S.L. performed the data analyses. All authors contributed to the writing of the manuscript.

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Correspondence to Stilianos Louca.

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Louca, S., Polz, M.F., Mazel, F. et al. Function and functional redundancy in microbial systems. Nat Ecol Evol 2, 936–943 (2018). https://doi.org/10.1038/s41559-018-0519-1

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