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Microbial substrate preference dictated by energy demand rather than supply

Nature Geoscience volume 10, pages 577–581 (2017)Cite this article

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Abstract

Growth substrates that maximize energy yield are widely thought to be utilized preferentially by microorganisms. However, observed distributions of microorganisms and their activities often deviate from predictions based solely on thermodynamic considerations of substrate energy supply. Here we present observations of the bioenergetics and growth yields of a metabolically flexible, thermophilic strain of the archaeon Acidianus when grown autotrophically on minimal medium with hydrogen (H2) or elemental sulfur (S°) as an electron donor, and S° or ferric iron (Fe3+) as an electron acceptor. Thermodynamic calculations indicate that S°/Fe3+ and H2/Fe3+ yield three- and fourfold more energy per mole of electrons transferred, respectively, than the H2/S° couple. However, biomass yields in Acidianus cultures provided with H2/S° were eightfold greater than when provided S°/Fe3+ or H2/Fe3+, indicating that the H2/S° redox couple is preferred. Indeed, cells provided with all three growth substrates (H2, Fe3+ and S°) grew preferentially by reduction of S° with H2. We conclude that substrate preference is dictated by differences in the energy demand of electron transfer reactions in Acidianus when grown with different substrates, rather than substrate energy supply.

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Figure 1: Electron micrographs of DS80 cells grown with different electron donor/acceptor pairs reveal differences in morphology.
Figure 2: Bioenergetics and biomass yields per kilojoule of energy dissipated in DS80 cultures provided with H2/S°, S°/Fe3+ or H2/Fe3+.
Figure 3: Growth and/or substrate transformation activities in biotic and abiotic experiments provided with H2/S°/Fe3+.

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Acknowledgements

This work was supported by National Science Foundation grant EAR-1123689 to E.S.B. and EAR-1123649 to E.L.S. and NASA Exobiology and Evolutionary Biology Grant (NNX13AI11G) to E.S.B. The NASA Astrobiology Institute is supported by grant NNA13AA94A to E.E.R. and E.S.B. and grant NNA15BB02A to E.L.S. and E.S.B. M.J.A. acknowledges support from the CONICYT Becas-Chile Scholarship program.

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Authors and Affiliations

  1. Department of Microbiology and Immunology, Montana State University, Bozeman, Montana, 59717, USA

    Maximiliano J. Amenabar & Eric S. Boyd

  2. School of Earth & Space Exploration and School of Molecular Sciences, Arizona State University, Tempe, Arizona, 85281, USA

    Everett L. Shock

  3. NASA Astrobiology Institute, Mountain View, California, 94035, USA

    Everett L. Shock, Eric E. Roden & Eric S. Boyd

  4. Department of Geosciences, University of Wisconsin, Madison, Wisconsin, 53706, USA

    Eric E. Roden

  5. Institute of Biological Chemistry, Washington State University, Pullman, Washington, 99164, USA

    John W. Peters

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  1. Maximiliano J. Amenabar
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Contributions

M.J.A. and E.S.B. designed and conducted the experiment. E.E.R. assisted with genomic sequencing. E.L.S. and E.E.R. assisted with bioenergetic calculations. All authors contributed to the writing of this paper.

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Correspondence to Eric S. Boyd.

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Amenabar, M., Shock, E., Roden, E. et al. Microbial substrate preference dictated by energy demand rather than supply. Nature Geosci 10, 577–581 (2017). https://doi.org/10.1038/ngeo2978

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