Closest relatives of poxviruses are spread in the gut of humans and animals worldwide: the egoviruses
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Abstract
Large and giant double-stranded DNA viruses within the phylum Nucleocytoviricota are diverse and prevalent in the environment where they substantially affect the ecology and evolution of eukaryotes 1–4 . Until now, these viruses were only sporadically found in the digestive system of vertebrates 5–7 . Here, we present the discovery of a diversified group of Nucleocytoviricota viruses dubbed egoviruses that almost exclusively occur in the digestive system of vertebrates worldwide. Egoviruses are most closely related to poxviruses and represent a third order within the class Pokkesviricetes 8 . They contain large linear genomes that include genes linked to multilayered icosahedral capsids only observed in asfuviruses. The widespread occurrence of egovirus genes in genomes of metamonads (with signal particularly enriched among Trichomonas and Tritrichomonas ), and their co-existence in human fecal samples as demonstrated by our metagenomic survey point towards a preferential infection of unicellular eukaryotes known to prevail, often as symbionts or pathogens, in the gut of vertebrates worldwide 9 . Notably, the numerous Egovirales genes found throughout Trichomonas vaginalis genomes (>3% of their gene pools) designate this prominent sexually transmitted human pathogen as a likely vector to the spread of egoviruses. Notably, one egovirus clade is human-specific, evolutionarily constrained, and spread across continents, demonstrating a long-term association with the human population at a global scale. Egoviruses represent the only diverse, widespread, and abundant group of double-stranded DNA viruses infecting eukaryotes in the digestive system of vertebrates, with implications for human health, capsid evolution and the origin of poxviruses.
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Data availability
Is your analysis code available (as a github repo or otherwise)?
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This methodology recovered 13 complete Egovirales genomes.
So essentially the RNAPolA needed to be on the same contig as the rest of the genes, so each of these 13 genomes is a single assembled contig? How do you check whether additional genes could be found on the edges of the contig that didn't assemble?
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We generated a custom diamond database91 (v.2.1.8) from this resource and summarized the taxonomic affiliation of each sequence in a complementary metadata file
Is this database available for re-use anywhere?
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Unicellular eukaryotes in Egovirales-positive metagenomic assembliesFinally, we assessed whether the detection of egoviruses in the gut samples coincides with the presence of any particular group of unicellular eukaryotes, which could serve as egovirus hosts. We identified eukaryotic RNApolA genes in 225 out of the 864 Egovirales-positive samples. Two clades accounted for nearly 95% of this signal: the genus Blastocystis (a Stramenopile) and a larger group of ciliates (Figure 3; Table S7). Blastocystis is highly prevalent in the digestive system of humans62–64 and various animals65,66, whereas ciliates are prevalent in the rumen microbiome of herbivorous mammals (e.g., cow, sheep, buffalo)67–70 and can also occur in other vertebrates such as pigs71,72. The limited eukaryotic diversity co-detected with egoviruses across metagenomic …
Unicellular eukaryotes in Egovirales-positive metagenomic assembliesFinally, we assessed whether the detection of egoviruses in the gut samples coincides with the presence of any particular group of unicellular eukaryotes, which could serve as egovirus hosts. We identified eukaryotic RNApolA genes in 225 out of the 864 Egovirales-positive samples. Two clades accounted for nearly 95% of this signal: the genus Blastocystis (a Stramenopile) and a larger group of ciliates (Figure 3; Table S7). Blastocystis is highly prevalent in the digestive system of humans62–64 and various animals65,66, whereas ciliates are prevalent in the rumen microbiome of herbivorous mammals (e.g., cow, sheep, buffalo)67–70 and can also occur in other vertebrates such as pigs71,72. The limited eukaryotic diversity co-detected with egoviruses across metagenomic assemblies suggests that Blastocystis and ciliates are the only two unicellular eukaryotic host candidates. Blastocystis was detected in 137 of the 864 Egovirales-positive samples, mainly in humans (n=65), pigs (n=52) and chicken (n=14). In addition, we only detected the ciliates in 87 out of 864 Egovirales-positive samples, mainly in pigs (n=40), cows (n=20) and buffalos (n=11). The correlation between the mean coverage of egoviruses and Blastocystis, ciliates, or the remaining eukaryotic signal found across all 864 Egovirales-positive samples was weak (Figure 4 and Table S8). In one striking example, the metagenome with the highest mean coverage for an egovirus (nearly 500X coverage in a chicken fecal sample) had no eukaryotic signal co-detected by means of our RNApolA survey. Overall, at the scale of all vertebrate species (Figures 3 and 4; Tables S5, S7 and S8), no clear patterns could be found among the metagenomic assemblies that would support one unicellular eukaryotic clade as being the prime host for egoviruses.
Is it possible that, with such narrow host ranges, these viruses are infecting human cells in a non-pathogenic way? As large double stranded DNA viruses, do you know if they participate in horizontal gene transfer with there hosts like poxviruses do? If they do, this might be one way to test host, seeing if whether there are genes in the virus that have a lot of structural similarity to different host candidates.
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