Microbial substrate preference dictated by energy demand, not supply

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°) as an electron donor, and S° or ferric iron (Fe(3+)) as an electron acceptor. Thermodynamic calculations indicate that S°/Fe(3+) and H(2)/Fe(3+) yield three- and four-fold more energy per mol electron transferred, respectively, than the H(2)/S° couple. However, biomass yields in Acidianus cultures provided with H(2)/S° were eight-fold greater than when provided S°/Fe(3+) or H(2)/Fe(3+), indicating the H(2)/S° redox couple is preferred. Indeed, cells provided with all three growth substrates (H(2), Fe(3+), and S°) grew preferentially by reduction of S° 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.