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Intracellular metabolite levels shape sulfur isotope fractionation during microbial sulfate respiration

Significance Microbes can discriminate among metabolites that differ only in the stable isotopes of the same element. This stable isotope fractionation responds systematically to environmental variables like extracellular metabolite concentrations and to physiological ones like cell-specific metabolic rates. These observable characteristics define a stable isotope phenotype, as exemplified by the rich database of experimental sulfur isotope fractionations from sulfate-respiring bacteria and archaea. We developed a quantitative model for sulfur isotope fractionation during sulfate respiration that incorporates only experimentally accessible biochemical information. With this approach, stable isotope phenotypes can be decomposed into their physiological, enzymatic, and environmental parts, potentially illuminating the relative influences of these components in natural microbial populations today, as well as how they may have varied in the deep past. We present a quantitative model for sulfur isotope fractionation accompanying bacterial and archaeal dissimilatory sulfate respiration. By incorporating independently available biochemical data, the model can reproduce a large number of recent experimental fractionation measurements with only three free parameters: (i) the sulfur isotope selectivity of sulfate uptake into the cytoplasm, (ii) the ratio of reduced to oxidized electron carriers supporting the respiration pathway, and (iii) the ratio of in vitro to in vivo levels of respiratory enzyme activity. Fractionation is influenced by all steps in the dissimilatory pathway, which means that environmental sulfate and sulfide levels control sulfur isotope fractionation through the proximate influence of intracellular metabolites. Although sulfur isotope fractionation is a phenotypic trait that appears to be strain specific, we show that it converges on near-thermodynamic behavior, even at micromolar sulfate levels, as long as intracellular sulfate reduction rates are low enough (<<1 fmol H2S⋅cell−1⋅d−1).