Extensive array of endogenous giant viral elements in a polar alga shows dynamic transcriptional response to abiotic stress

Giant viruses, members of the phylum Nucleocytoviricota (NCV), possess exceptionally large genomes that encode hundreds of genes involved in replication, metabolism, and host manipulation. These viruses have emerged as major players in protist ecology and evolution. Recent studies reveal that their genomes are frequently endogenized in protists, contributing to structural innovation and functional novelty. Yet, the extent and impact of such events on genome architecture and physiological responses in algae inhabiting extreme polar environments remain unknown. Here, we report widespread giant endogenous viral elements (GEVEs) in nine polar microalgae, revealing extensive viral integration. Most notably, Chlamydomonas sp. ICE-L, an Antarctic sea ice alga, harbors over 400 GEVE regions spanning more than 26 megabase pairs (Mbp)-the most extensive giant viral endogenization recorded in any eukaryote. These insertions, derived from multiple NCV lineages, encode >25,000 genes, including those associated with replication, chromatin remodeling, stress responses, and transposable elements. Transcriptomic analyses show that ∼40% of GEVE genes are actively expressed, with hundreds being differentially regulated under UV radiation, salinity, and temperature stress. A co-expression network reveals modular regulation patterns, suggesting functional integration of viral genes into host transcriptional networks. Additionally, phylogeny supports giant viruses as important mediators of horizontal gene transfer (HGT) of key freeze-tolerance proteins, such as ice-binding proteins (IBPs), in polar algae. Our findings position giant viral endogenization as a key driver of genome content, regulatory complexity, and environmental adaptation in polar algae and establish Chlamydomonas sp. ICE-L as a model for studying virus-derived genomic innovation in extreme environments.