Hydrogen gas oxidation-driven reductive dissolution of solid-phase arsenic contributing to arsenite pollution in groundwater: Insights from metagenomic and microcosm analyses

Abstract

Hydrogen gas (H₂) is naturally generated by biological and non-biological reactions in various environmental niches. However, the influence of H₂ on microbial processes that cause the mobilization and discharge of arsenic from solids into groundwater remains to be resolved. Given that As^V-respiring prokaryotes (ARPs) have been demonstrated to significantly contribute to the formation of As-polluted groundwater, our study specifically examined the interactions between H₂ and ARPs. We prepared an ARPs-enriched culture from As-polluted soils. Metagenomic analyses of the ARP population revealed that approximately 46.7% of the qualified ARPs' MAGs contain at least one type I Ni-Fe hydrogenase. The Ni-Fe hydrogenase proteins in ARPs show unique diversity. Functional assays indicate that the ARP population exhibited notable activity in oxidizing H₂ while concurrently reducing As^V under strictly anoxic conditions. Arsenic release assays indicate that the ARP population is highly proficient at catalyzing the reductive mobilization of arsenic in scorodite, utilizing hydrogen as the electron donor. These findings offer the initial evidence that H₂ can directly promote the formation of arsenic-polluted groundwater mediated by ARPs, a biogeochemical process that has long been overlooked. Therefore, this study enhances our insight into the microbial mechanisms involved in the generation of arsenic-polluted groundwater.