Giant viruses: spore‐like missing links between Rickettsia and mitochondria?

Abstract

Phyloproteomics indicate common viral origin from ancient cells before archaea, bacteria, and eukaryota split and subsequent size and complexity reductions occurred. Further independent evidence for the cellular origin of viruses is reviewed for the virus order Megavirales, focusing on the family Poxviridae. Megavirales comprises giant viruses, double‐stranded DNA viruses whose genomes exceed some bacterial ones and large enough to parasitize large‐celled protists (amoeba). Giant viruses, virophages, and mitochondria have homologous DNA and RNA polymerases and share RNA splicing punctuation by stem–loop hairpins. Giant virus factories and amoeban mitochondria colocate, with viral proteins homologous to mitochondrial proteins specifically targeting mitochondrial inner membranes. Mitochondria share asexual budding with many bacterial endospores and membrane‐enveloped viruses. These megavirus−mitochondrion similarities are not coincidental: systematic alignment analyses have detected candidate megaviral homologs of each amoeban mitogene (including ribosomal RNAs) distributed across megaviral genomes. These candidate megaviral homologs overall follow mitogene order, and megaviral−mitogenome synteny increases with viral genome reduction. This analysis is repeated within Poxviridae, whose organellar‐like morphogenesis is reminiscent of mitochondria. More generally, the results confirm the patterns observed in Megavirales: synteny with amoeban mitogenomes increases with genome reduction. Parsimoniously interpreting this suggests Megavirales and mitochondria have a rickettsia‐like common ancestor. Megavirales could be the missing links between bacterial‐like cells and mitochondria, implying cellular‐to‐viral‐to‐subcellular macroevolution.

Syntenies Between Cohosted Mitochondrial, Chloroplast, and Phycodnavirus Genomes: Functional Mimicry and/or Common Ancestry?

“…In addition, pieces of eukaryotic nucleus-and mitogenomeencoded ribosomal RNAs were detected in various viruses belonging to Megavirales (Abrahão et al, 2018;Seligmann and Raoult, 2018;Seligmann, 2018aSeligmann, , 2019. Mitochondrial rRNA remnants seem most widely distributed within Megavirales (Seligmann, 2018a(Seligmann, , 2019, suggesting that giant viruses have mitochondrion-like ancestors. Viral candidates for rRNA homologs apparently decay faster than viral homolog candidates of other mitogenes (Seligmann, 2018a), in line with rRNA absence in viruses.…”

“…Viral candidates for rRNA homologs apparently decay faster than viral homolog candidates of other mitogenes (Seligmann, 2018a), in line with rRNA absence in viruses. However, megaviral candidate homologs of mitogenes tend to conserve the mitochondrial gene order, and these synteny levels between megaviral and mitochondrial genomes increase with viral genome size reduction, when comparing megaviral families at large (within each small and large genome size groups, Seligmann, 2018a) and when comparing genomes of Poxviridae (Seligmann, 2019).…”

“…Previous analyses used a single mitogenome as reference to test synteny between mitogenomes and megaviral genomes, the mitogenome of Acanthamoeba castellanii (Seligmann 2018a(Seligmann , 2019. To test whether positive results on synteny with viruses are circumstantial, due to mitogene arrangements in that specific mitogenome, synteny analyses for Phycodnaviridae were done using additional reference mitogenomes, notably 8 mitogenomes from hosts infected by Phycodnaviridae, and the human mitogenome, a total of 10 mitogenomes.…”

“…The morphogenesis of some viruses among Poxviridae resembles that of cellular subcompartments, suggesting that some viruses might have originated from cells and/or cellular compartments (Bandea, 2009a(Bandea, , 2009b. Recent analyses suggest that at least some viruses, the giant viruses (Megavirales) (Colson et al, 2013) might have evolved from bacteria-and/or mitochondria-like cells (Seligmann, 2018a(Seligmann, , 2019. Indeed, several properties of mitochondria, and especially mitogenomes, are reminiscent of viruses.…”

Testing for correlation between traits under directional evolution

“…Correlation tests may concern any kind of traits: phenotypic, genetic or other. For instance, Seligmann (2018Seligmann ( , 2019 observed a correlation between the syntheny level of poxviruses with amoeban mitogenome and their genome size. Assessing the correlation between two traits measured on several species cannot be performed by directly computing the Pearson correlation coefficient on the traits values since these values are not independent but related through the evolutionary relationships of the species involved (Diaz-Uriarte and Garland 1996).…”