Diversity and Salinity Adaptations of Ammonia Oxidizing Archaea in Three Estuaries of China

Ammonia-oxidizing archaea (AOA) are ubiquitously found in diverse habitats and play pivotal roles in the nitrogen and carbon cycle, especially in estuarine and coastal environments. Despite the fact that the diversity and distribution of AOA are thought to be tightly linked to habitats, little is known about the relationship that underpins their genomic traits, adaptive potentials, and ecological niches. Here, we have characterized and compared the AOA community in three estuaries of China using metagenomics. AOA were the dominant ammonia oxidizers in the three estuaries. Through phylogenetic analyses, five major AOA groups were identified, including the Nitrosomarinus-like, Nitrosopumilus-like, Aestuariumsis-like, Nitrosarchaeum-like, and Nitrosopelagicus-like groups. Statistical analyses showed that the aquatic and sedimentary AOA communities were mainly influenced by spatial factors (latitude and water depth) and environmental factors (salinity, pH, and dissolved oxygen) in estuaries, respectively. Compared to AOA dwelling in terrestrial and marine habitats, estuarine AOA encoded more genes involved in glucose and amino acid metabolism, transport systems, osmotic control, and cell motility. The low proteome isoelectric points (pI), high content of acidic amino acids, and the presence of potassium ion and mechanosensitive channels suggest a "salt-in" strategy for estuarine AOA to counteract high osmolarity in their surroundings. Our findings have indicated potential adaptation strategies and highlighted their importance in the estuarine nitrogen and carbon cycles. KEY POINTS: • Spatial and environmental factors influence water and sediment AOA respectively. • Estuarine AOA share low proteome isoelectric value and high acid amino acids content. • AOA adaptation to estuaries is likely resulted from their unique genomic features.