Insights into the Evolutionary and Ecological Roles of Bathyarchaeia in Arsenic Detoxification

Arsenic (As) is a prevalent toxic element, posing significant risks to organisms, including microbes. While microbial arsenic detoxification has been extensively studied in bacteria, archaeal mechanisms remain understudied. Here, we investigated arsenic resistance genes in Bathyarchaeia, one of the most abundant archaeal lineages on Earth. Comprehensive genomic analysis of 318 Bathyarchaeia representatives revealed a widespread distribution of arsenic resistance genes, with 60% of genomes harboring genes for arsenate reduction (arsR1 and arsC2), arsenite methylation (arsM), and arsenic transport (acr3, arsP, and arsB). Phylogenetic analysis revealed that these genes are widely distributed across 14 archaeal phyla, including Asgardarchaeota, Thermoproteota, and Thermoplasmatota, with close evolutionary relationships among these archaeal lineages. In situ investigation of sediment columns and laboratory microcosm experiments demonstrated a strong positive correlation between Bathyarchaeia abundance and arsenic concentrations, suggesting their adaptation to arsenic-rich environments. Molecular dating analysis placed the emergence of Bathyarchaeia at approximately 3.01 billion years ago, with the evolution of their arsenic resistance mechanisms closely tracking major geological events, including the Great Oxidation Event (2.4-2.1 Gya), Huronian Glaciation (2.29-2.25 Gya), and Cryogenian Glaciation (∼700 Mya). Our findings highlight the critical role of Archaea in the arsenic cycle and provide insights into the evolutionary history of arsenic resistance associated with paleogeochemical changes in Bathyarchaeia.