Evolution and Diversity of the <em>Microviridae</em> Viral Family through a Collection of 81 New Complete Genomes Assembled from Virome Reads

<div><p>Recent studies suggest that members of the <em>Microviridae</em> (a family of ssDNA bacteriophages) might play an important role in a broad spectrum of environments, as they were found in great number among the viral fraction from seawater and human gut samples. 24 completely sequenced <em>Microviridae</em> have been described so far, divided into three distinct groups named <em>Microvirus</em>, <em>Gokushovirinae</em> and <em>Alpavirinae</em>, this last group being only composed of prophages. In this study, we present the analysis of 81 new complete <em>Microviridae</em> genomes, assembled from viral metagenomes originating from various ecosystems. The phylogenetic analysis of the core genes highlights the existence of four groups, confirming the three sub-families described so far and exhibiting a new group, named <em>Pichovirinae</em>. The genomic organizations of these viruses are strikingly coherent with their phylogeny, the <em>Pichovirinae</em> being the only group of this family with a different organization of the three core genes. Analysis of the structure of the major capsid protein reveals the presence of mushroom-like insertions conserved within all the groups except for the microviruses. In addition, a peptidase gene was found in 10 <em>Microviridae</em> and its analysis indicates a horizontal gene transfer that occurred several times between these viruses and their bacterial hosts. This is the first report of such gene transfer in <em>Microviridae</em>. Finally, searches against viral metagenomes revealed the presence of highly similar sequences in a variety of biomes indicating that <em>Microviridae</em> probably have both an important role in these ecosystems and an ancient origin.</p>