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Growth rate as a link between microbial diversity and soil biogeochemistry

Nature Ecology & Evolution (2024)Cite this article

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Abstract

Measuring the growth rate of a microorganism is a simple yet profound way to quantify its effect on the world. The absolute growth rate of a microbial population reflects rates of resource assimilation, biomass production and element transformation—some of the many ways in which organisms affect Earth’s ecosystems and climate. Microbial fitness in the environment depends on the ability to reproduce quickly when conditions are favourable and adopt a survival physiology when conditions worsen, which cells coordinate by adjusting their relative growth rate. At the population level, relative growth rate is a sensitive metric of fitness, linking survival and reproduction to the ecology and evolution of populations. Techniques combining omics and stable isotope probing enable sensitive measurements of the growth rates of microbial assemblages and individual taxa in soil. Microbial ecologists can explore how the growth rates of taxa with known traits and evolutionary histories respond to changes in resource availability, environmental conditions and interactions with other organisms. We anticipate that quantitative and scalable data on the growth rates of soil microorganisms, coupled with measurements of biogeochemical fluxes, will allow scientists to test and refine ecological theory and advance process-based models of carbon flux, nutrient uptake and ecosystem productivity. Measurements of in situ microbial growth rates provide insights into the ecology of populations and can be used to quantitatively link microbial diversity to soil biogeochemistry.

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Fig. 1: Methods for measuring soil microbial growth rates in situ.
Fig. 2: Relative growth rates of soil microbial assemblages and individual taxa in multiple ecosystems.

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Acknowledgements

We appreciate discussion with members of the Center for Ecosystem Science and Society and Lawrence Livermore National Laboratory (LLNL) Soil Microbiome Scientific Focus Area team. This work was supported by grants from the US Department of Energy’s (DOE’s) Biological Systems Science Division Program in Genomic Science (DE-SC0020172 and DE-SC0023126) and the DOE’s Office of Biological and Environmental Research Genomic Science Program (LLNL Microbes Persist Soil Microbiome Scientific Focus Area SCW1632). A.P. is grateful for support from the National Science Foundation (NSF; 1643871). B.W.G.S. is grateful for support from the Linus Pauling Distinguished Postdoctoral Fellowship programme through the Pacific Northwest National Laboratory. E.M. is grateful for support from the NSF (2114570) and D.O.E.’s Biological Systems Science Division Program in Genomic Science (SC0016207). M.M.F. is grateful for support from the DOE’s Science Graduate Student Research Program. Work at the LLNL was conducted under the auspices of the US DOE under contract DE-AC52-07NA27344. N.F. is grateful for support from the NSF (AW5809-826664).

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Authors and Affiliations

  1. Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA

    Megan M. Foley, Benjamin J. Koch, Paul Dijkstra, Michaela Hayer, Michelle Mack, Jane Marks, Rebecca L. Mau, Victoria Monsaint-Queeney, Jeffrey Propster, Alicia Purcell, Egbert Schwartz & Bruce A. Hungate

  2. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA

    Megan M. Foley, Benjamin J. Koch, Paul Dijkstra, Michaela Hayer, Michelle Mack, Jane Marks, Rebecca L. Mau, Victoria Monsaint-Queeney, Jeffrey Propster, Alicia Purcell, Egbert Schwartz & Bruce A. Hungate

  3. Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, USA

    Bram W. G. Stone & Kirsten Hofmockel

  4. Department of Geological Sciences, University of Colorado Boulder, Boulder, CO, USA

    Tristan A. Caro

  5. Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA

    Noah W. Sokol, Steven J. Blazewicz & Jennifer Pett-Ridge

  6. Department of Ecology, Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Brianna K. Finley

  7. Division of Plant and Soil Sciences, West Virginia University, Morgantown, WV, USA

    Ember Morrissey

  8. Department of Biology, New Mexico Highlands University, Las Vegas, NM, USA

    Jeffrey Propster

  9. Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA

    Alicia Purcell

  10. Life & Environmental Sciences Department, University of California, Merced, Merced, CA, USA

    Jennifer Pett-Ridge

  11. Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, CO, USA

    Noah Fierer

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

    Noah Fierer

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Contributions

M.M.F., B.J.K., T.A.C., N.F. and B.A.H. conceived of the study idea. M.M.F., B.W.G.S., B.J.K. and B.A.H. designed the study methodology and performed the formal analysis. M.M.F., B.W.G.S., B.J.K., S.J.B., P.D., M.H., K.H., B.K.F., J.M., R.L.M., V.M.-Q., E.M., J.P., A.P. and N.F. performed the investigation. M.M.F., B.W.G.S. and B.A.H. curated the data. M.M.F. and B.A.H. visualized the data. S.J.B., K.H., E.M., E.S., J.P.-R. and B.A.H. acquired the funding. S.J.B., K.H., E.M., E.S., J.P.-R. and B.A.H. provided resources. J.P.-R. and B.A.H. supervised the project and performed project administration. M.M.F., B.J.K., T.A.C., N.W.S., N.F. and B.A.H. wrote the manuscript. All authors reviewed and edited the manuscript.

Corresponding author

Correspondence to Megan M. Foley.

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Nature Ecology & Evolution thanks Carla Cruz-Paredes, Jörg Schnecker and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Methods and Tables 1 and 2.

Supplementary Data 1

Published estimates of in situ growth rates of soil microbial assemblages.

Supplementary Data 2

Published estimates of in situ growth rates of soil bacterial phyla measured via H218O qSIP.

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Foley, M.M., Stone, B.W.G., Caro, T.A. et al. Growth rate as a link between microbial diversity and soil biogeochemistry. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02520-7

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