Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids
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)...
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| Published in: | Nature communications Vol. 10; no. 1; pp. 3425 - 12 |
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| Main Authors: | , , , |
| Format: | Journal Article |
| Language: | English |
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Nature Publishing Group UK
31.07.2019
Nature Publishing Group Nature Portfolio |
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| ISSN: | 2041-1723, 2041-1723 |
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| 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.
Most single-stranded DNA viruses have small genomes replicated by rolling circle mechanism which is initiated by the Rep protein. Here, using sequence similarity network and phylogenetic analyses, Kazlauskas et al. show that viral Reps evolved from Reps of bacterial and archaeal plasmids on multiple independent occasions. |
|---|---|
| AbstractList | 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. 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. Most single-stranded DNA viruses have small genomes replicated by rolling circle mechanism which is initiated by the Rep protein. Here, using sequence similarity network and phylogenetic analyses, Kazlauskas et al. show that viral Reps evolved from Reps of bacterial and archaeal plasmids on multiple independent occasions. 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.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. 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. 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. Most single-stranded DNA viruses have small genomes replicated by rolling circle mechanism which is initiated by the Rep protein. Here, using sequence similarity network and phylogenetic analyses, Kazlauskas et al. show that viral Reps evolved from Reps of bacterial and archaeal plasmids on multiple independent occasions. Most single-stranded DNA viruses have small genomes replicated by rolling circle mechanism which is initiated by the Rep protein. Here, using sequence similarity network and phylogenetic analyses, Kazlauskas et al. show that viral Reps evolved from Reps of bacterial and archaeal plasmids on multiple independent occasions. |
| ArticleNumber | 3425 |
| Author | Krupovic, Mart Koonin, Eugene V. Kazlauskas, Darius Varsani, Arvind |
| Author_xml | – sequence: 1 givenname: Darius orcidid: 0000-0001-6135-8549 surname: Kazlauskas fullname: Kazlauskas, Darius organization: Institute of Biotechnology, Life Sciences Center, Vilnius University – sequence: 2 givenname: Arvind orcidid: 0000-0003-4111-2415 surname: Varsani fullname: Varsani, Arvind organization: The Biodesign Center for Fundamental and Applied Microbiomics, School of Life Sciences, Center for Evolution and Medicine, Arizona State University, Structural Biology Research Unit, Department of Integrative Biomedical Sciences, University of Cape Town, Rondebosch – sequence: 3 givenname: Eugene V. orcidid: 0000-0003-3943-8299 surname: Koonin fullname: Koonin, Eugene V. organization: National Center for Biotechnology Information, National Library of Medicine. National Institutes of Health – sequence: 4 givenname: Mart orcidid: 0000-0001-5486-0098 surname: Krupovic fullname: Krupovic, Mart email: krupovic@pasteur.fr organization: Department of Microbiology, Institut Pasteur |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31366885$$D View this record in MEDLINE/PubMed https://hal.science/hal-02242067$$DView record in HAL |
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J. doi: 10.1186/s12985-018-0923-9 |
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| Snippet | 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... Most single-stranded DNA viruses have small genomes replicated by rolling circle mechanism which is initiated by the Rep protein. Here, using sequence... |
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| SubjectTerms | 631/181/735 631/326/596 631/337 Archaea - genetics Bacteria Bacteria - genetics Base Sequence Biological evolution Deoxyribonucleic acid DNA DNA Helicases - genetics DNA viruses DNA, Single-Stranded - genetics DNA, Viral - genetics Endonuclease Evolution, Molecular Genes Genome, Viral - genetics Genomes Humanities and Social Sciences Life Sciences multidisciplinary Origins Papillomaviridae Papillomaviridae - genetics Parvovirus - genetics Parvoviruses Phylogeny Plasmids Plasmids - genetics Polyomavirus - genetics Recombination Replication RNA viruses Science Science (multidisciplinary) Sequence Alignment Single-stranded DNA Viruses |
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| Title | Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids |
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