A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

Abstract

Here we report the discovery of Yaravirus, a new lineage of amoebal virus with a puzzling origin and phylogeny. Yaravirus presents 80 nm-sized particles and a 44,924 bp dsDNA genome encoding for 74 predicted proteins. More than 90% (68) of Yaravirus predicted genes have never been described before, representing ORFans. Only six genes had distant homologs in public databases: an exonuclease/recombinase, a packaging-ATPase, a bifunctional DNA primase/polymerase and three hypothetical proteins. Furthermore, we were not able to retrieve viral genomes closely related to Yaravirus in 8,535 publicly available metagenomes spanning diverse habitats around the globe. The Yaravirus genome also contained six types of tRNAs that did not match commonly used codons. Proteomics revealed that Yaravirus particles contain 26 viral proteins, one of which potentially representing a novel capsid protein with no significant homology with NCLDV major capsid proteins but with a predicted double-jelly roll domain. Yaravirus expands our knowledge of the diversity of DNA viruses. The phylogenetic distance between Yaravirus and all other viruses highlights our still preliminary assessment of the genomic diversity of eukaryotic viruses, reinforcing the need for the isolation of new viruses of protists.Significance statementMost of the known viruses of amoeba have been seen to share many features that eventually prompted authors to classify them into common evolutionary groups. Here we describe Yaravirus, an entity that could represent either the first isolated virus of Acanthamoeba spp. out of the group of NCLDVs or, in alternative evolutive scenario, it is a distant and extremely reduced virus of this group. Contrary to what is observed in other isolated viruses of amoeba, Yaravirus is not represented by a large/giant particle and a complex genome, but at the same time carries an important number of previously undescribed genes, including one encoding a novel major capsid protein. Metagenomic approaches also testified for the rarity of Yaravirus in the environment.

Global Organization and Proposed Megataxonomy of the Virus World

“…The "yaravirus" genome shares several distinctive genes (e.g., those encoding DJR-MCP, packaging ATPase, and primase-S3H) with NCLDVs whereas others are apparently lacking. The provenance of this unusual virus remains to be established through detailed genome analysis (238).…”

efam: an expanded, metaproteome-supported HMM profile database of viral protein families

“… Forterre, 2011 ; Howard-Varona et al , 2020 ; Roux et al , 2016 ), as well as identifying viral hallmark genes that increase the confidence in detecting previously unseen viruses in metagenomic sequences (see category 1 viruses in VirSorter; Roux et al , 2015a ). Problematically, viral gene annotation has proved to be challenging as the field has a history of observing that most viral genes in metagenomes typically cannot be annotated ( Boratto et al , 2020 ; Gregory et al , 2019 ; Roux et al , 2016 , 2019b ). Part of this lack of annotation is due to challenges of scaling annotation, which limits many studies to interrogating against only a single functional annotation database like KEGG or VOGDB.…”

Structural Stability of Optofluidic Nanostructures in Flow-Through Operation

“…A trendy and increasingly demanded approach to in situ sensing is the use of lab-on-a-chip platforms enabled by cell phones to record, analyze, and transmit the results [2][3][4]. With the recent emergence of new pathogens, such as the Coronavirus and the Yaravirus, an on-site analysis will limit their health impact with a rapid sensing test, quantifying the severity of the infection, and assisting with the quarantine measures [5,6]. Periodic arrays of subwavelength structures fabricated in metal films enable surface plasmon resonance (SPR), which motivated their use as biosensors for several applications in different fields [7][8][9][10][11][12].…”