Insights into the Evolutionary and Ecological Roles of <i>Bathyarchaeia</i> 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 <i>Bathyarchaeia</i>, one of the most abundant archaeal lineages on Earth. Comprehensive genomic analysis of 318 <i>Bathyarchaeia</i> representatives revealed a widespread distribution of arsenic resistance genes, with 60% of genomes harboring genes for arsenate reduction (<i>arsR1</i> and <i>arsC2</i>), arsenite methylation (<i>arsM</i>), and arsenic transport (<i>acr3</i>, <i>arsP</i>, and <i>arsB</i>). Phylogenetic analysis revealed that these genes are widely distributed across 14 archaeal phyla, including <i>Asgardarchaeota</i>, <i>Thermoproteota</i>, and <i>Thermoplasmatota</i>, with close evolutionary relationships among these archaeal lineages. In situ investigation of sediment columns and laboratory microcosm experiments demonstrated a strong positive correlation between <i>Bathyarchaeia</i> abundance and arsenic concentrations, suggesting their adaptation to arsenic-rich environments. Molecular dating analysis placed the emergence of <i>Bathyarchaeia</i> 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 <i>Bathyarchaeia</i>.