Gene Acquisition Convergence between Entomopoxviruses and Baculoviruses

Abstract

Organisms from diverse phylogenetic origins can thrive within the same ecological niches. They might be induced to evolve convergent adaptations in response to a similar landscape of selective pressures. Their genomes should bear the signature of this process. The study of unrelated virus lineages infecting the same host panels guarantees a clear identification of phyletically independent convergent adaptation. Here, we investigate the evolutionary history of genes in the accessory genome shared by unrelated insect large dsDNA viruses: the entomopoxviruses (EPVs, Poxviridae) and the baculoviruses (BVs). EPVs and BVs have overlapping ecological niches and have independently evolved similar infection processes. They are, in theory, subjected to the same selective pressures from their host’s immune responses. Their accessory genomes might, therefore, bear analogous genomic signatures of convergent adaption and could point out key genomic mechanisms of adaptation hitherto undetected in viruses. We uncovered 32 homologous, yet independent acquisitions of genes originating from insect hosts, different eukaryotes, bacteria and viruses. We showed different evolutionary levels of gene acquisition convergence in these viruses, underlining a continuous evolutionary process. We found both recent and ancient gene acquisitions possibly involved to the adaptation to both specific and distantly related hosts. Multidirectional and multipartite gene exchange networks appear to constantly drive exogenous gene assimilations, bringing key adaptive innovations and shaping the life histories of large DNA viruses. This evolutionary process might lead to genome level adaptive convergence.

The Apis mellifera Filamentous Virus Genome

“…Likewise, the ribonucleotide reductase IgC domain of AmFV_116 ORF clustered with poxviruses and herpesviruses ( Figure 4 ). This pattern is consistent with networks of multiple horizontal gene transfers (HGT) between viruses infecting the same host, or gene acquisition from the host or its microbiota [ 41 , 57 ]. Indeed, many genes in the AmFV genome have putative viral or bacterial homologues, such as the Bro genes, while others are homologues of insect genes, such as the AmFV_12 ORF which has a kinesin domain also present in Drosophila pseudoobscura , and the AmFV_36 ORF which has homologies with the precursor of pacifastin venom protein 1 of Nasonia vitripenis ( Table S3 , nr database).…”

“…Other elements typical of baculoviruses that were also found in the AmFV genome are the Bro genes, of which at least six were found in the AmFV genome. BRO proteins, whose functions are still unknown, contain a DNA binding domain and belong to a multigene family that is wide spread among large insect viruses, including entomopoxviruses and iridoviruses, as well as in dsDNA phage and prokaryotic class II transposons [ 40 , 41 ].…”

“…Kinesin belongs to a class of motor proteins that has been shown to facilitate intracellular trafficking of viral components along the microtubule cytoskeleton [ 49 , 50 ]. The presence of a putative homologue of an insect cellular gene in the AmFV genome suggests that AmFV may have evolved a mutualistic association with its host, involving horizontal transfer of genes between host and virus, as it is known to occur with certain other large DNA viruses, such as Bracoviruses [ 37 , 51 ], Baculoviruses and Poxviruses [ 41 ]. This possibility requires more detailed investigations.…”

The Complete Genome Sequence of a Second Distinct Betabaculovirus from the True Armyworm, Mythimna unipuncta

“…Previous analysis of viral and host dut genes from a variety of sources supports the horizontal transfer of dut genes from host to virus genomes and the subsequent duplication, deletion and movement of dut genes within viral genomes [50]. Two comprehensive phylogenetic analyses of baculovirus dut genes have been published recently [51, 52]. Both analyses indicate that baculovirus dut genes do not constitute a monophyletic group, but likely originate from multiple sources.…”

A novel cypovirus found in a betabaculovirus co-infection context contains a poxvirus immune nuclease (poxin)-related gene

“…Viruses have multiple independent origins [39], hence, the study of unrelated virus lines infecting the same group of hosts are important to comprehend and identify independent convergent base adaptations supported by fundamental genomic adaptive mechanisms not yet detected in eukaryotic viruses [40]. Great examples are CPVs and baculoviruses (BVs), which share a convergent strategy to protect their virions from environment, the production of an OB.…”