Electron carriers in microbial sulfate reduction inferred from experimental and environmental sulfur isotope fractionations

Abstract

Dissimilatory sulfate reduction (DSR) has been a key process influencing the global carbon cycle, atmospheric composition and climate for much of Earth's history, yet the energy metabolism of sulfate-reducing microbes remains poorly understood. Many organisms, particularly sulfate reducers, live in low-energy environments and metabolize at very low rates, requiring specific physiological adaptations. We identify one such potential adaptation-the electron carriers selected for survival under energy-limited conditions. Employing a quantitative biochemical-isotopic model, we find that the large S isotope fractionations (>55‰) observed in a wide range of natural environments and culture experiments at low respiration rates are only possible when the standard-state Gibbs free energy (ΔG'°) of all steps during DSR is more positive than -10 kJ mol. This implies that at low respiration rates, only electron carriers with modestly negative reduction potentials are involved, such as menaquinone, rubredoxin, rubrerythrin or some flavodoxins. Furthermore, the constraints from S isotope fractionation imply that ferredoxins with a strongly negative reduction potential cannot be the direct electron donor to S intermediates at low respiration rates. Although most sulfate reducers have the genetic potential to express a variety of electron carriers, our results suggest that a key physiological adaptation of sulfate reducers to low-energy environments is to use electron carriers with modestly negative reduction potentials.The ISME Journal advance online publication, 31 October 2017; doi:10.1038/ismej.2017.185.

A Critical Look at the Combined Use of Sulfur and Oxygen Isotopes to Study Microbial Metabolisms in Methane-Rich Environments

“…Naturally, as the cell specific sulfate reduction rates in the environment are 2–6 orders of magnitude lower than this calculation, e.g., ( Holmkvist et al, 2011 ), turnover of intracellular metabolites increases from seconds to minutes or hours and the oxygen isotope effect becomes significant. These findings are also in agreement with the finding that low csSRR which produce large sulfur isotope fractionations (such as the ones observed in the environment) can only be driven by modestly negative electron carriers (i.e., menaquinone) whereas very negative electron carriers (i.e., ferredoxins) restrict the net fractionation to around < 22‰ ( Wenk et al, 2017 ). In most cases, SALP is a direct consequence of these intracellular states.…”

Theoretical estimates of equilibrium carbon and hydrogen isotope effects in microbial methane production and anaerobic oxidation of methane

“…Bioisotopic models have the potential to reveal details of the elusive mechanisms that control such isotopic fingerprints. Such models have been successfully applied to microbial sulfate reduction by demonstrating how the sulfur isotope fractionations of individual steps in the pathway combine to control the net fractionation (Wing & Halevy, 2014;Zaarur et al, 2017;Wenk et al, 2017).…”

Role of APS reductase in biogeochemical sulfur isotope fractionation

“…3b). Because the Δ G of the Apr reaction should have near-zero values to accommodate the wide range of naturally occurring fractionation, Wenk et al 54 recently proposed that sulfate respiration relies primarily on electron carriers with modestly negative redox potential such as menaquinone (MQH 2 /MQ, E °′ = −75mV). Although such a small difference between the redox potentials of electron carriers and APS (APS/HSO 3 − , E °′ = −60 mV) can contribute to maintaining reversibility in APS reduction and thereby produce larger isotope fractionation, such low energy yields make it difficult to account for the energy needed to generate a proton gradient that is presumed to be coupled to the oxidation of membrane-bound electron carriers 55,56 .…”