Genomic Comparison of Closely Related Giant Viruses Supports an Accordion-like Model of Evolution

Genome gigantism occurs so far in Phycodnaviridae and Mimiviridae (order Megavirales). Origin and evolution of these Giant Viruses (GVs) remain open questions. Interestingly, availability of a collection of closely related GV genomes enabling genomic comparisons offer the opportunity to better understand the different evolutionary forces acting on these genomes. Whole genome alignment for five groups of viruses belonging to the Mimiviridae and Phycodnaviridae families show that there is no trend of genome expansion or general tendency of genome contraction. Instead, GV genomes accumulated genomic mutations over the time with gene gains compensating the different losses. In addition, each lineage displays specific patterns of genome evolution. Mimiviridae (megaviruses and mimiviruses) and Chlorella Phycodnaviruses evolved mainly by duplications and losses of genes belonging to large paralogous families (including movements of diverse mobiles genetic elements), whereas Micromonas and Ostreococcus Phycodnaviruses derive most of their genetic novelties thought lateral gene transfers. Taken together, these data support an accordion-like model of evolution in which GV genomes have undergone successive steps of gene gain and gene loss, accrediting the hypothesis that genome gigantism appears early, before the diversification of the different GV lineages.