Article

Microbial substrate preference dictated by energy demand rather than supply

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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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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.

Author information

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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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Eric S. Boyd.

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