Purifying selection and low recombination facilitated sequential colonization of benthic and pelagic coastal ocean by ammonia-oxidizing archaea

The evolutionary adaptation of archaea to ecologically diverse habitats remains poorly understood. Ammonia-oxidizing archaea (AOA) exhibit significant diversification across various environmental conditions; however, their ecological dynamics, diversification, and associated evolutionary processes are still largely unexplored in coastal environments, which contain extensive ecosystem heterogeneity. Combining newly assembled metagenomic data from Chinese marginal seas (2,059 km coverage) with global datasets (spanning over 16,000 km), these knowledge gaps were explored across a continental-scale latitudinal gradient. It revealed that coastal AOA genomic diversity is latitude-dependent, with predicted optimum growth temperatures and substrate metabolic pathways explaining the geographical distribution. The two dominant genus-level clades exhibited significantly distinct benthic-pelagic niches, associated with specific genes involved in nutrient uptake and stress resistance. Phylogenomic reconstructions suggest that AOA initially colonized the coastal ocean sediments around 718 million years ago (Mya), and subsequent purifying selection and low recombination facilitated the AOA niche expansion into marine coastal environments. By revealing the evolutionary trajectories of Nitrososphaeria and their differential colonization patterns, our findings offer a novel perspective on the mechanisms of AOA diversification in the coastal ocean. This work advances our understanding of microbial diversification and niche differentiation of AOA in coastal ecosystems as well as the evolutionary forces shaping their global biogeography.