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.

中文翻译：

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隐藏的基因组多样性驱动世界性真核超微型浮游植物的生态位划分


海洋真核浮游植物是海洋食物网的基础，但缺乏参考基因组或仅代表一个分类单元的单个基因组导致了对其分类、适应性和功能多样性的低估。在这里，我们将菌株分离与宏基因组分箱相结合，以从世界性超微型浮游植物深球藻属（传统上被认为是单特异性的）中恢复基因组。我们对 37 个深球藻基因组的恢复和分析描绘了它们的全球基因组多样性，并建立了四个进化枝（BI、BII、BIII、BIV）。我们的宏基因组丰度调查揭示了每个进化枝分化良好的生态位和独特的生物地理分布，主要由温度、盐度和养分可用性决定。比较基因组学分析进一步揭示了分支特异性基因组特征，这些特征支撑了生态位适应并有助于深球菌的全球流行。我们的研究结果强调温度是该属基因组多样化的主要驱动因素，进化枝的分歧与影响其当代热生态位的主要古气候事件相一致。此外，极地适应进化枝中C2H2锌指和锚蛋白重复基因家族的独特富集表明海洋真核浮游植物中以前未被认识的冷适应机制。我们的研究提供了这种重要的真核超微型浮游植物的全面基因组图谱，深入了解其微观多样性和响应不断变化的环境的适应性进化。