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Abstract

Giant Viruses of amoebas, recently classified in the class Megaviricetes, are a group of viruses that are able to infect major eukaryotic lineages. How viral insertions shape the structure and evolution of the invaded genomes is unclear, but it is known that the unprecedented functional potential of giant viruses is the result of an intense genetic interplay with their hosts.
We previously identified a set of giant virus sequences in the genome of P. parasitica, an oomycete and major devastating plant pathogen. Here, we show that viral pieces are found in a 550-kb locus and are organized in three main clusters. Viral sequences like RNA polymerases I and II and major capsid protein were identified, along with orphan sequences, as a hallmark of GV insertions. Mining of public databases and phylogenetic reconstructions suggest an ancient association of oomycetes and giant viruses of amoeba including faustoviruses, African swine fever virus (ASFV) and pandoraviruses, and that a single viral insertion occurred early in the evolutionary history of oomycetes, prior to the Phytophthora-Pythium radiation, estimated to ~80 MY ago. Functional annotation reveals that the viral insertions are located into a gene sparse region of the Phytophthora genome, characterized by a plethora of Transposable Elements, effectors and other genes potentially involved in virulence.
Transcription of viral genes was investigated through analysis of RNA-Seq data and qPCR experiments. We show that most viral genes are not expressed, and that a variety of mechanisms including deletions, Transposable Elements insertions and RNA interference could contribute to transcriptional repression. However, a gene coding a truncated copy of RNA polymerase II has been shown to be expressed in a wide range of physiological conditions, including responses to stress, along with a set of neighboring sequences. These results, which describe for the first time the endogenization of a giant virus in an oomycete, contribute to challenge our view of Phytophthora evolution.