Hidden genomic diversity drives niche partitioning in a cosmopolitan eukaryotic picophytoplankton

Marine eukaryotic phytoplankton are fundamental to the marine food web, yet the lack of reference genomes or just a single genome representing a taxon has led to an underestimation of their taxonomic, adaptive, and functional diversity. Here, we integrated strain isolation with metagenomic binning to recover genomes from the cosmopolitan picophytoplankton genus Bathycoccus, traditionally considered monospecific. Our recovery and analysis of 37 Bathycoccus genomes delineated their global genomic diversity and established four evolutionary clades (BI, BII, BIII, BIV). Our metagenomic abundance survey revealed well-differentiated ecological niches and distinct biogeographic distributions for each clade, predominantly shaped by temperature, salinity, and nutrient availability. Comparative genomics analyses further revealed clade-specific genomic traits, that underpin niche adaptation and contribute to the global prevalence of Bathycoccus. Our findings underscore temperature as a major driver of genome diversification in this genus, with clade divergences coinciding with major paleoclimatic events that influenced their contemporary thermal niches. Moreover, the unique enrichment of C2H2 zinc finger and ankyrin repeat gene families in polar-adapted clades suggests previously unrecognized cold-adaptation mechanisms in marine eukaryotic phytoplankton. Our study offers a comprehensive genomic landscape of this crucial eukaryotic picophytoplankton, providing insights into their microdiversity and adaptive evolution in response to changing environments.