Genome reduction in marine ammonia-oxidizing archaea driven by elevated temperature

Marine ammonia-oxidizing archaea (AOA) have evolved into diverse lineages and ecological niches. However, less is known about the impact of environmental factors on their genomic evolution. By integrating 281 AOA metagenome-assembled genomes (MAGs) around global oceans, we revealed that AOA genome size decreased with elevated temperature across the two predominant genera Nitrosopumilus and Nitrosopelagicus. This was supported by their contrasting temperature preferences, with the large-genome Nitrosopumilus commonly occupying cold waters and the genome-reduced Nitrosopelagicus preferring warm waters. We further found a warm-like subclade diverging from the cold-adapted Nitrosopumilus and a cold-like subclade from the warm-adapted Nitrosopelagicus. These divergences were accompanied by the enrichment of functional genes associated with adaptation to temperature fluctuation. Our results highlight the role of temperature in shaping genomic reduction and phylogenetic divergence in marine AOA, with implications for nitrogen cycling under ocean warming.