Comparative Genomics and Environmental Distribution of Large dsDNA Viruses in the Family Asfarviridae

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.

High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System

“…One Pimascovirales virus (GVMAG-M-3300009467-15) and one Asfuvirales virus (GVMAG-M-3300027833-19) were also abundant in the transcriptomes, suggesting they may also infect microbial eukaryotes in the community. The Asfuvirales virus found here was also recently identified in waters off the coast of South Africa ( 7 ), indicating that it may be broadly distributed in the ocean. The presence of numerous divergent families of Nucleocytoviricota in the metatranscriptomes supports the view that marine systems harbor an immense diversity of these viruses that are actively infecting a wide variety of protists hosts.…”

“…A recently proposed taxonomy of this viral phylum delineated 6 orders and 32 families ( 5 ), including the previously established families Asfarviridae , Poxviridae , Marseilleviridae , Iridoviridae , Phycodnaviridae , and Mimiviridae . Members of the Nucleocytoviricota are known to infect a broad range of eukaryotic hosts; members of the Poxviridae and Iridoviridae families infect numerous metazoans; members of the Imitervirales and Algavirales orders infect a wide range of algae and other protists; and members of the Asfuvirales infect a mixture of metazoan and protist hosts ( 6 – 10 ). Members of the Nucleocytoviricota typically harbor exceptionally large genomes that are often >300 kbp in length, and in some cases as large as 2.5 Mbp ( 9 ).…”

A phylogenomic framework for charting the diversity and evolution of giant viruses

“…The recognized taxonomic ranks in this phylum currently include 2 classes, 5 orders, 7 families, and 41 genera. The viruses in the families Asfarviridae, Ascoviridae, Iridoviridae, and Poxviridae infect metazoans, whereas those in the families Marseilleviridae, Mimiviridae, and Phycodnaviridae primarily infect algae or heterotrophic unicellular eukaryotes [6][7][8]. Members of the Nucleocytoviricota span an exceptionally broad range of genome sizes, from below 100 kbp to more than 2.5 Mbp.…”

A Phylogenomic Framework for Charting the Diversity and Evolution of Giant Viruses

“…This phylum currently includes two classes that encompasses five orders with seven recognized and several additional, proposed families. The viruses in the families Poxviridae, Asfarviridae, and Iridoviridae infect metazoans, whereas those in the families Mimiviridae, Phycodnaviridae and Marseilleviridae as well as several putative families primarily infect algae or heterotrophic unicellular eukaryotes [5][6][7].The members of the Nucleocytoviricota span an exceptionally broad range of genome sizes…”