Comparative Genomics of Chrysochromulina Ericina Virus and Other Microalga-Infecting Large DNA Viruses Highlights Their Intricate Evolutionary Relationship with the Established Mimiviridae Family

International audienceChrysochromulina Ericina Virus CeV-01B was isolated from Norwegian coastal waters in 1998. Its icosahedral particle is 160 nm in diameter and encloses a 474-kb dsDNA genome. This virus, although infecting a microalgae (the haptophycea Haptolina ericina, formerly Chrysochromulina ericina), is phylogenetically related to members of the Mimiviridae family, initially established with the acanthamoeba-infecting Mimivirus and Megavirus as prototypes. This family was latter split into two genera (Mimivirus and Cafetariavirus) following the characterization of a virus infecting the heterotrophic stramenopile Cafeteria roenbergensis (CroV). CeV, as well as two of its close relatives infecting the unicellular photosynthetic eukaryotes Phaeocystis globosa (PgV) and Aureococcus anophagefferens (AaV), are currently unclassified by ICTV. The detailed comparative analysis of the CeV genome presented here confirms the phylogenetic affinity of this emerging group of microalgae-infecting viruses with the Mimiviridae, but argue in favor of their classification inside a distinct clade within the family. Although CeV, PgV, AaV share more common features between them than with the larger Mimiviridae, they also exhibit a large complement of unique genes attesting of their complex evolutionary history. We identified several gene fusion events and cases of convergent evolution involving independent lateral gene acquisitions. Finally, CeV possesses an unusual number of inteins, some of which are closely related despite been inserted in non-homologous genes. This appears to contradict the paradigm of allele-specific inteins and suggests that Mimiviridae might be especially efficient in spreading inteins while enlarging their repertoire of homing genes