Interchromosomal translocations and large deletions drive the evolution of the outlier chromosome in the smallest photosynthetic eukaryote

Marine microalgal populations can rapidly evolve resistance to viruses upon infection. In Ostreococcus mediterraneus resistance to the prasinovirus OmV2 emerged within five days in all virus-exposed populations. Whole-genome sequencing of pairs of resistant and susceptible cell lines revealed extensive structural genomic changes, particularly on the Small Outlier Chromosome (SOC). SOC alterations included large deletions, duplications, rearrangements, and whole chromosome duplication, yet no consistent structural variant or single nucleotide polymorphism was directly associated with resistance. Hybrid de novo assemblies confirmed the unique SOC assembly of each strain, with a highly polymorphic ∼2 kb tandem repeat region exhibiting an "accordion-like" pattern of expansion and contraction. No new viral insertions were found, though endogenous viral elements were conserved across lines. Two interchromosomal translocations between the SOC and chromosomes 2 and 17 offer novel insights into the mechanisms underlying the distinctive evolutionary path of this chromosome. Together, these findings demonstrate that resistance to OmV2 evolves rapidly and consistently but cannot yet be attributed to any specific structural variations, suggesting that transcriptional or post-transcriptional mechanisms underly the resistant phenotype. Instead, the high rate of localized genomic structural variations points to a distinct mechanism of chromosome evolution.