Microbial substrate preference dictated by energy demand rather than 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 (H₂) or elemental sulfur (S^o) as an electron donor, and S^o or ferric iron (Fe³⁺) as an electron acceptor. Thermodynamic calculations indicate that S^o/Fe³⁺ and H₂/Fe³⁺ yield three- and fourfold more energy per mole of electrons transferred, respectively, than the H₂/S^o couple. However, biomass yields in Acidianus cultures provided with H₂/S^o were eightfold greater than when provided S^o/Fe³⁺ or H₂/Fe³⁺, indicating that the H₂/S^o redox couple is preferred. Indeed, cells provided with all three growth substrates (H₂, Fe³⁺ and S^o) grew preferentially by reduction of S^o 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.