Loss of replication and transcription systems accompanying transition to nucleus-dependent replication in “Ariadnavirales”, a proposed new order in nucleocytoviricot class Megaviricetes

Abstract

Sicyoidochytrium minutum DNA virus (SmDNAV) was isolated several years ago from a protist host of family Thraustochytriaceae of the class Labyrinthulomycetes. This virus shared little similarity to other viruses in gene content and protein sequences, albeit seemingly belonging to the phylum Nucleocytoviricota. By extensive searches in genomic and metagenomic sequence databases, we identified numerous long contigs related to the SmDNAV genome and analyzed proteins shared by these putative viruses. Phylogenetic analyses place these viruses within the class Megaviricetes, outside of all established orders, and as a sister group to the clade combining families Mamonoviridae and ”Manesviridae”. Homologs of SmDNAV proteins were found in association (either integrated or co-sequenced) with other Labyrinthulomycetes and Rhodophyta protists from diverse marine and freshwater environments. Consequently, we propose SmDNAV as the prototype member of a new order, provisionally named “Ariadnavirales”, within class Megaviricetes, phylum Nucleocytoviricota. Members of “Ariadnavirales” have lost most of the genes encoding components of the replication and transcription systems that are otherwise conserved in nucleocytoviricots, suggestive of transition to genome replication and expression dependent on the host nucleus. Importance The viral phylum Nucleocytoviricota consists of diverse viruses with double-stranded DNA genomes within a broad size range from about 40 kilobases to about 5 megabases. The great majority of nucleocytoviricots encode DNA and RNA polymerases, and other proteins involved in genome replication and expression, and are known or predicted to replicate within viral ‘factories’ in the host cell cytoplasm. In recent years, several new groups of nucleocytoviricots have been discovered, primarily, by metagenome mining. Here we describe a putative new order of nucleocytoviricots, which we provisionally name “Ariadnavirales” for their protist hosts. These viruses have lost most of the genes responsible for genome replication and expression in other nucleocytoviricots, and their replication apparently depends on the host nucleus.