Abstract
The family Asfarviridae is a group of nucleo-cytoplasmic large DNA viruses (NCLDVs) of which African swine fever virus (ASFV) is well-characterized. Recently the discovery of several Asfarviridae members other than ASFV has suggested that this family represents a diverse and cosmopolitan group of viruses, but the genomics and distribution of this family have not been studied in detail. To this end we analyzed five complete genomes and 35 metagenome-assembled genomes (MAGs) of viruses from this family to shed light on their evolutionary relationships and environmental distribution. The Asfarvirus MAGs derive from diverse marine, freshwater, and terrestrial habitats, underscoring the broad environmental distribution of this family. We present phylogenetic analyses using conserved marker genes and whole-genome comparison of pairwise average amino acid identity (AAI) values, revealing a high level of genomic divergence across disparate Asfarviruses. Further, we found that Asfarviridae genomes encode genes with diverse predicted metabolic roles and detectable sequence homology to proteins in bacteria, archaea, and eukaryotes, highlighting the genomic chimerism that is a salient feature of NCLDV. Our read mapping from Tara oceans metagenomic data also revealed that three Asfarviridae MAGs were present in multiple marine samples, indicating that they are widespread in the ocean. In one of these MAGs we identified four marker genes with > 95% AAI to genes sequenced from a virus that infects the dinoflagellate Heterocapsa circularisquama (HcDNAV). This suggests a potential host for this MAG, which would thereby represent a reference genome of a dinoflagellate-infecting giant virus. Together, these results show that Asfarviridae are ubiquitous, comprise similar sequence divergence as other NCLDV families, and include several members that are widespread in the ocean and potentially infect ecologically important protists.
Highlights
The nucleo-cytoplasmic large DNA viruses (NCLDVs), called Nucleocytoviricota, comprise a phylum of dsDNA viruses that infect diverse eukaryotes (Van Etten et al, 2010b; Koonin et al, 2020)
Amoebae have been used as an effective system to cultivate many NCLDV, recent cultivation-independent studies have discovered a wide range of these viruses in diverse environments, suggesting that uncultivated members of this viral phylum are ubiquitous in the biosphere and infect diverse hosts (Monier et al, 2008; Hingamp et al, 2013; Bäckström et al, 2019; Endo et al, 2020; Moniruzzaman et al, 2020a; Schulz et al, 2020)
We assess the phylogenetic relationship of these new metagenome-assembled genomes (MAGs) and previously discovered Asfarviruses to explore their evolutionary relationships, and we identify the potential evolutionary origins of the Asfarviridae genomic repertoires
Summary
The nucleo-cytoplasmic large DNA viruses (NCLDVs), called Nucleocytoviricota, comprise a phylum of dsDNA viruses that infect diverse eukaryotes (Van Etten et al, 2010b; Koonin et al, 2020). A culture independent study in early 2020 reported Asfar-like virus (AbalV) causing mass mortality in abalone (Matsuyama et al, 2020) Together, these studies have begun to show that the Asfarviridae are likely a diverse family of NCLDV that are globally distributed and infect both protist and metazoan hosts. Two studies (Moniruzzaman et al, 2020a; Schulz et al, 2020) reported numerous new metagenome-assembled genomes (MAGs) of NCLDV, some of which have phylogenetic affinity with the Asfarviridae family. We assess the distribution of marine Asfarvirus genomes in the ocean, and we identified high sequence similarity between one marine Asfarvirus MAG to marker gene sequences available from a virus known to infect the dinoflagellate Heterocapsa circularisquama, suggesting a potential host for this MAG. Our findings reveal that the Asfarviridae members are widespread in the ocean and potentially have roles in biogeochemical cycling through infection of ecologically-important protist lineages
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