Phaeocystales, comprising the genus Phaeocystis and an uncharacterized sister lineage, are nanoplanktonic haptophytes widespread in the global ocean. Several species form mucilaginous colonies and influence key biogeochemical cycles, yet their underlying diversity and ecological strategies remain underexplored. Here, we present new genomic data from 13 strains, including three high-quality reference genomes (N50 > 30 kbp), and integrate previous metagenome-assembled genomes to resolve a robust phylogeny. Divergence timing of P. antarctica aligns with Miocene cooling and Southern Ocean isolation. Genomic traits reveal metabolic flexibility, including mixotrophic nitrogen acquisition in temperate waters and gene expansions linked to polar nutrient adaptation. Concordantly, transcriptomic comparisons between temperate and polar Phaeocystis suggest Southern Ocean populations experience iron and B12 limitation. We also identify signatures of horizontal gene transfer and endogenous giant virus/virophage insertions. Together, these findings highlight Phaeocystales as an ecologically versatile and geographically widespread lineage shaped by evolutionary innovation and adaptation to contrasting environmental stressors.

ARC Centre of Excellence in Synthetic Biology Macquarie University Sydney Australia

Biology Centre of the Czech Academy of Sciences Institute of Parasitology České Budějovice Czech Republic

Cell and Plant Physiology Laboratory CNRS CEA INRAE IRIG Université Grenoble Alpes 38054 Grenoble France

Center for Microbiome Innovation University of California San Diego La Jolla CA USA

Department of Bioengineering University of California San Diego La Jolla CA USA

Department of Earth and Environmental Sciences Rutgers University Newark Newark NJ USA

Department of Freshwater and Marine Ecology Institute for Biodiversity and Ecosystem Dynamics University of Amsterdam Amsterdam The Netherlands

Department of Pediatrics University of California San Diego La Jolla CA USA

Department of Plant and Microbial Biology University of California Berkeley Berkeley CA USA

European Molecular Biology Laboratory 69117 Heidelberg Germany

Genome Sequencing Center HudsonAlpha Institute for Biotechnology Huntsville AL USA

Hollings Marine Laboratory College of Charleston Charleston SC USA

Institut de Biologie de l'École Normale Supérieure CNRS Paris UK

Microbial and Environmental Genomics J Craig Venter Institute La Jolla CA USA

NIOZ Royal Netherlands Institute for Sea Research Den Burg The Netherlands

Program in Materials Science and Engineering University of California San Diego La Jolla CA USA

School of Natural Sciences Macquarie University Sydney Australia

Scripps Institution of Oceanography University of California San Diego La Jolla CA USA

Skidaway Institute of Oceanography University of Georgia Savannah GA USA

Stanford University Department of Earth System Science Stanford CA USA

Station Biologique de Roscoff CNRS Sorbonne Université Roscoff France

United States Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA USA

Université Paris Saclay INRAE AgroParisTech Institute Jean Pierre Bourgin for Plant Sciences 78000 Versailles France

Université Paris Saclay INRAE Institute of Plant Sciences Paris Saclay Gif sur Yvette France

Université Paris Saclay INRAE URGI 78026 Versailles France

University of South Bohemia České Budějovice Czech Republic

University of South Florida St Petersburg FL USA

University of Southern California Los Angeles CA USA

Woods Hole Oceanographic Institution Woods Hole MA USA

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