Genome Analysis of the First Marseilleviridae Representative from Australia Indicates that Most of Its Genes Contribute to Virus Fitness

The family Marseilleviridae consists of Acanthamoeba-infecting large DNA viruses with icosahedral particles ∼ 0.2 μm in diameter and genome sizes in the 346- to 380-kb range. Since the isolation of Marseillevirus from a cooling tower in Paris (France) in 2009, the family Marseilleviridae has expanded rapidly, with representatives from Europe and Africa. Five members have been fully sequenced that are distributed among 3 emerging Marseilleviridae lineages. One comprises Marseillevirus and Cannes 8 virus, another one includes Insectomime virus and Tunisvirus, and the third one corresponds to the more distant Lausannevirus. We now report the genomic characterization of Melbournevirus, the first representative of the Marseilleviridae isolated from a freshwater pond in Melbourne, Australia. Despite the large distance separating this sampling point from France, Melbournevirus is remarkably similar to Cannes 8 virus and Marseillevirus, with most orthologous genes exhibiting more than 98% identical nucleotide sequences. We took advantage of this optimal evolutionary distance to evaluate the selection pressure, expressed as the ratio of nonsynonymous to synonymous mutations for various categories of genes. This ratio was found to be less than 1 for all of them, including those shared solely by the closest Melbournevirus and Cannes 8 virus isolates and absent from Lausannevirus. This suggests that most of the 403 protein-coding genes composing the large Melbournevirus genome are under negative/purifying selection and must thus significantly contribute to virus fitness. This conclusion contrasts with the more common view that many of the genes of the usually more diverse large DNA viruses might be (almost) dispensable.