Oxygen-driven divergence of marine group II archaea reflected by transitions of superoxide dismutases

The superoxide anion radical (O2 center dot-), the primary reactive oxygen species (ROS), is detrimental to cellular functions. Marine group II (MGII) archaea predominantly inhabit surface ocean environments that are rich in ROS; however, their defense mechanisms against ROS damage remain unknown. In this study, we integrated the analyses of archaeal 16S rRNA gene amplicons and metagenome-assemblage genomes of MGII archaea from the northern South China Sea and 250 other previously published MGII genomes to investigate their antioxidant mechanisms. The results show that the proportion of oxygen-promoted MGII operational taxonomic units in the iron/manganese superoxide dismutase (Fe/MnSOD) gene-containing group was significantly higher than that in the nickel SOD (NiSOD) group, suggesting that MGII members with Fe/MnSOD may have superior antioxidant capacity relative to members possessing NiSOD. Molecular clock analysis of MGII genomes revealed frequent species divergence correlating to the differentiation of Fe/MnSOD or NiSOD genes. The acquisition/loss of these genes in the MGII genomes was synchronized with the historical changes in atmospheric oxygen and oceanic metal element concentrations over the last 2.4 billion years, suggesting that variations in the antioxidant capacity of MGII archaea in response to changing oxygen levels may have driven their divergences over time.IMPORTANCEReactive oxygen species (ROS), including superoxide anion, is a series of substances that cause oxidative stress for all organisms. Marine group II (MGII) archaea are mainly live in the surface seawater and exposed to considerable ROS. Therefore, it is important to understand the antioxidant capacity of MGII. Our research found that Fe/Mn- superoxide dismutase (Fe/MnSOD) may be more suitable for MGII to resist oxidative damage, and the changes in oxygen concentrations and SOD metallic cofactors play an important role in the selection of SOD by the 17 clades of MGII, which in turn affects the species differentiation of MGII. Overall, this study provides insight into the co-evolutionary history of these uncultivated marine archaea with the earth system. Reactive oxygen species (ROS), including superoxide anion, is a series of substances that cause oxidative stress for all organisms. Marine group II (MGII) archaea are mainly live in the surface seawater and exposed to considerable ROS. Therefore, it is important to understand the antioxidant capacity of MGII. Our research found that Fe/Mn- superoxide dismutase (Fe/MnSOD) may be more suitable for MGII to resist oxidative damage, and the changes in oxygen concentrations and SOD metallic cofactors play an important role in the selection of SOD by the 17 clades of MGII, which in turn affects the species differentiation of MGII. Overall, this study provides insight into the co-evolutionary history of these uncultivated marine archaea with the earth system.