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 (H-2) or elemental sulfur (S degrees) as an electron donor, and S degrees or ferric iron (Fe3+) as an electron acceptor. Thermodynamic calculations indicate that S degrees/Fe3+ and H-2/Fe3+ yield three-and fourfold more energy per mole of electrons transferred, respectively, than the H-2/S degrees couple. However, biomass yields in Acidianus cultures provided with H-2/S degrees were eightfold greater than when provided S degrees/Fe3+ or H-2/Fe3+, indicating that the H-2/S degrees redox couple is preferred. Indeed, cells provided with all three growth substrates (H-2, Fe3+ and S degrees) grew preferentially by reduction of S degrees with H-2. 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.