Prochlorococcus is the key primary producer in marine ecosystems, and the high-light-adapted clade II (HLII) is the most abundant ecotype. However, the genomic and ecological basis of Prochlorococcus HLII in the marine environment has remained elusive. Here, we show that the ecologically coherent subclade differentiation of HLII corresponds to genomic and ecological characteristics on the basis of analyses of 31 different strains of HLII, including 12 novel isolates. Different subclades of HLII with different core and accessory genes were identified, and their distribution in the marine environment was explored using the TARA Oceans metagenome database. Three major subclade groups were identified, viz., the surface group (HLII-SG), the transition group (HLII-TG), and the deep group (HLII-DG). These subclade groups showed different temperature ranges and optima for distribution. In regression analyses, temperature and nutrient availability were identified as key factors affecting the distribution of HLII subclades. A 35% increase in the relative abundance of HLII-SG by the end of the 21st century was predicted under the Representative Concentration Pathway 8.5 scenario. Our results show that the ubiquity and distribution of Prochlorococcus HLII in the marine environment are associated with the differentiation of diverse subclades. These findings provide insights into the large-scale shifts in the Prochlorococcus community in response to future climate change. IMPORTANCEProchlorococcus is the most abundant oxygenic photosynthetic microorganism on Earth, and high-light-adapted clade II (HLII) is the dominant ecotype. However, the factors behind the dominance of HLII in the vast oligotrophic oceans are still unknown. Here, we identified three distinct groups of HLII subclades, viz., the surface group (HLII-SG), the transition group (HLII-TG), and the deep group (HLII-DG). We further demonstrated that the ecologically coherent subclade differentiation of HLII corresponds to genomic and ecological characteristics. Our study suggests that the differentiation of diverse subclades underlies the ubiquity and distribution of Prochlorococcus HLII in the marine environment and provides insights into the shifts in the Prochlorococcus community in response to future climate change.
Keywords: Prochlorococcus HLII; metagenome; pangenome; subclade differentiation.