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. 2019 Jul 31;10(1):3425.
doi: 10.1038/s41467-019-11433-0.

Multiple Origins of Prokaryotic and Eukaryotic Single-Stranded DNA Viruses From Bacterial and Archaeal Plasmids

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Free PMC article

Multiple Origins of Prokaryotic and Eukaryotic Single-Stranded DNA Viruses From Bacterial and Archaeal Plasmids

Darius Kazlauskas et al. Nat Commun. .
Free PMC article

Abstract

Single-stranded (ss) DNA viruses are a major component of the earth virome. In particular, the circular, Rep-encoding ssDNA (CRESS-DNA) viruses show high diversity and abundance in various habitats. By combining sequence similarity network and phylogenetic analyses of the replication proteins (Rep) belonging to the HUH endonuclease superfamily, we show that the replication machinery of the CRESS-DNA viruses evolved, on three independent occasions, from the Reps of bacterial rolling circle-replicating plasmids. The CRESS-DNA viruses emerged via recombination between such plasmids and cDNA copies of capsid genes of eukaryotic positive-sense RNA viruses. Similarly, the rep genes of prokaryotic DNA viruses appear to have evolved from HUH endonuclease genes of various bacterial and archaeal plasmids. Our findings also suggest that eukaryotic polyomaviruses and papillomaviruses with dsDNA genomes have evolved via parvoviruses from CRESS-DNA viruses. Collectively, our results shed light on the complex evolutionary history of a major class of viruses revealing its polyphyletic origins.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Representative HUH superfamily Reps clustered by their pairwise sequence similarity. Lines connect sequences with P-value ≤ 1e−08. Groups were named after well-characterized plasmids, viruses or most frequent taxon
Fig. 2
Fig. 2
Diversity of viral-like Rep proteins in bacteria. a Phylogenetic tree of bacterial Rep proteins and their homologs in P. pulchra. Closely related sequences are collapsed to triangles, whose side lengths are proportional to the distances between closest and farthest leaf nodes. b CLANS groups of bacterial Rep proteins and their homologs. Nodes indicate protein sequences. Lines represent sequence relationships (CLANS P-value ≤ 1e−05). The nodes belonging to the same cluster are colored with the same colors, corresponding to the clades shown in panel A. c Genome maps of integrated and extrachromosomal plasmids representing groups 1–9. Homologous genes are depicted using the same color and their functions are listed on the right side of the figure
Fig. 3
Fig. 3
Conserved sequence motifs of Rep proteins. Bacterial Rep groups are depicted in gray background. Residues are colored by their chemical properties (polar, green; basic, blue; acidic, red; hydrophobic, black; neutral, purple). The Rep groups were manually ordered according to the pairwise similarity in the aligned motifs. The HUH endonuclease and SF3 helicase domains are delineated at the top of the figure
Fig. 4
Fig. 4
Relationships between Superfamily 3 helicases and AAA+ ATPases. a Superfamily 3 helicase and AAA+ ATPase domains clustered by their pairwise similarity using CLANS. In total, 3854 sequences were clustered with CLANS (CLANS P-value ≤ 5e−09). Groups of unclassified CRESS-DNA viruses are referred to as CRESSV1 through CRESSV6 (ref. ). b A proposed evolutionary scenario for the origin and evolution of viral Superfamily 3 helicases. Abbreviations: SF3, superfamily 3 helicase domain; HUH, HUH superfamily nuclease domain; OBD, origin-binding domain; HGT, horizontal gene transfer; RHR, rolling-hairpin replication
Fig. 5
Fig. 5
Maximum likelihood phylogenetic tree of Rep proteins. GasCSV—Gastropod-associated circular ssDNA virus. The tree was constructed with PhyML. Branches with support values below 70 are contracted
Fig. 6
Fig. 6
A proposed evolutionary scenario for the origin of CRESS-DNA viruses from bacterial plasmids. The three hypothetical events of CRESS-DNA virus emergence are indicated with numbered circles. JRC, jelly-roll capsid protein-encoding genes. Non-orthologous JRC genes are indicated with different colors

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