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Prochlorococcus 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. 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. IMPORTANCE Prochlorococcus 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.

The picocyanobacteria genera Prochlorococcus and Synechococcus play a significant role globally, dominating the primary production in warm and oligotrophic tropical and subtropical areas, which represent the largest oceanic ecosystem. Genomic studies have revealed high microdiversity within these genera. It is anticipated that ocean warming may cause decreased biodiversity in marine tropical areas, as increasing temperatures may lead to the development of a new thermal niche in these regions. Thus, our study aimed to characterize the microdiversity of picocyanobacteria in the Red Sea, one of the warmest oligotrophic seas on the planet, which is experiencing warming at a rate that exceeds the global average. We identified picocyanobacteria microdiversity in the open waters of the Eastern Red Sea basin, where seawater temperatures ranged from 22.2 to 32.4°C throughout the water column (from surface to 160 m depth). Both Prochlorococcus and Synechococcus populations were characterized to deep taxonomic levels, applying amplicon sequencing targeting the petB gene, revealing up to 15 different (sub)clades. Synechococcus dominated the basin, representing an average of 68.8% of the total reads assigned to both cyanobacteria. The subclade Synechococcus IIa and Prochlorococcus clade HLII were ubiquitous in the water column of the Eastern Red Sea basin, representing 73% and 56% of the Synechococcus and Prochlorococcus assigned reads, respectively. Maximum cyanobacteria richness was observed at approximately 27.5°C, declining at higher and lower temperatures (polynomial fit, R 2 = 0.2, p<0.0001). Synechococcus IIa dominated in the warmest surface waters (>30°C) of the Red Sea, displacing other (sub)clades to more saline and nutrient-poor waters, thereby reducing community diversity (polynomial fit, R 2 = 0.77, p<0.0001). Our study contributes to identifying changes in picocyanobacterial diversity when exposed to temperatures exceeding current oceanic thermal limits, through the analysis of Red Sea communities already inhabiting such higher-temperature niches.