DescriptionAll life on Earth is dependent on biologically mediated electron transfer (i.e., redox) reactions that are not at thermodynamic equilibrium. Biological redox reactions originally evolved in prokaryotes and ultimately, over the first ~ 2.5 billion years of Earth’s history, formed a global electronic circuit. To maintain the circuit on a global scale requires that oxidants and reductants be transported; the two major planetary electron conductors that connect global metabolism are geological fluids - primarily the atmosphere and the oceans. Because all organisms exchange gases with the environment, the evolution of redox reactions has been a major force in modifying the chemistry at Earth’s surface. First, a review is given of the discovery and consequences of redox reactions in microbes with a specific focus on the co-evolution of life and geochemical phenomena. With the larger picture in mind, the focus is then directed specifically to one of the earliest metabolic pathways on Earth. The reduction of elemental sulfur. is an important energy-conserving pathway in prokaryotes inhabiting geothermal environments, where sulfur respiration contributes to sulfur biogeochemical cycling. Despite this, the pathways through which elemental sulfur is reduced to hydrogen sulfide remain unclear in most microorganisms. We integrated growth experiments using Thermovibrio ammonificans, a deep-sea vent thermophile that conserves energy from the oxidation of hydrogen and reduction of both nitrate and elemental sulfur, with comparative transcriptomic and proteomic approaches, coupled with scanning electron microscopy. Our results revealed that two members of the FAD-dependent pyridine nucleotide disulfide reductase family, similar to sulfide-quinone reductase (SQR) and to NADH-dependent sulfur reductase (NSR), respectively, are over-expressed during sulfur respiration. Scanning electron micrographs and sulfur sequestration experiments indicated that direct access of T. ammonificans to sulfur particles strongly promoted growth. The sulfur metabolism of T. ammonificans appears to require abiotic transition from bulk elemental sulfur to polysulfide to nanoparticulate sulfur at an acidic pH, coupled to biological hydrogen oxidation. A coupled biotic-abiotic mechanism for sulfur respiration is put forward, mediated by an NSR-like protein as the terminal reductase.