Rhodoquinone-dependent electron transport chain is essential forC. eleganssurvival in hydrogen sulfide environments

Abstract

AbstractHydrogen sulfide (H2S) has traditionally been considered as an environmental toxin for animal lineages; yet, it plays a signaling role in various processes at low concentrations. Mechanisms controlling H2S in animals, especially in sulfide-rich environments, are not fully understood. The main detoxification pathway involves the conversion of H2S into less harmful forms, through a mitochondrial oxidation pathway. The first step of this pathway oxidizes sulfide and reduces ubiquinone (UQ) through sulfide-quinone oxidoreductase (SQRD/SQOR). Because H2S inhibits cytochrome oxidase and hence UQ regeneration, this pathway becomes compromised at high H2S concentrations. The free-living nematodeC. elegansfeeds on bacteria and can face high sulfide concentrations in its natural environment. This organism has an alternative ETC that uses rhodoquinone (RQ) as the lipidic electron transporter and fumarate as the final electron acceptor. In this study, we demonstrate that RQ is essential for survival in sulfide. RQ-less animals (kynu-1andcoq-2eKO) cannot survive high H2S concentrations, while UQ-less animals (clk-1andcoq-2aKO) exhibit recovery, even when provided with a UQ-deficient diet. Our findings highlight thatsqrd-1uses both benzoquinones and that RQ-dependent ETC confers a key advantage (RQ regeneration) over UQ in sulfide conditions.C. elegansalso faces cyanide, another cytochrome oxidase inhibitor, whose detoxification leads to H2S production, viacysl-2. Our study reveals that RQ delays killing by the HCN-producing bacteriaPseudomonas aeruginosaPAO1. These results underscore the fundamental role that RQ-dependent ETC serves as a biochemical adaptation to H2S environments, and to pathogenic bacteria producing cyanide and H2S toxins.