Unveiling Crucivirus Diversity by Mining Metagenomic Data
ABSTRACT The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viruses that encode capsid proteins that are most closely relat...
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American Society for Microbiology
2020
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oai:doaj.org-article:c83420450bfa44719ee6e8cbfc278d912021-11-15T16:19:08ZUnveiling Crucivirus Diversity by Mining Metagenomic Data10.1128/mBio.01410-202150-7511https://doaj.org/article/c83420450bfa44719ee6e8cbfc278d912020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01410-20https://doaj.org/toc/2150-7511ABSTRACT The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viruses that encode capsid proteins that are most closely related to those encoded by RNA viruses in the family Tombusviridae. The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of capsid genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and 10 capsid-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode. Most of the variation is reflected in the replication-associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins and that the exchange of Rep protein domains between cruciviruses is rarer than intergenic recombination. Additionally, we suggest members of the stramenopiles/alveolates/Rhizaria supergroup as possible crucivirus hosts. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses. IMPORTANCE Viruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Circular Rep-encoding single-stranded (CRESS) DNA viruses are ubiquitous in nature, many are agriculturally important, and they appear to have multiple origins from prokaryotic plasmids. A subset of CRESS-DNA viruses, the cruciviruses, have homologues of capsid proteins encoded by RNA viruses. The genetic structure of cruciviruses attests to the transfer of capsid genes between disparate groups of viruses. However, the evolutionary history of cruciviruses is still unclear. By collecting and analyzing cruciviral sequence data, we provide a deeper insight into the evolutionary intricacies of cruciviruses. Our results reveal an unexpected diversity of this virus group, with frequent recombination as an important determinant of variability.Ignacio de la HigueraGeorge W. KasunEllis L. TorranceAlyssa A. PrattAmberlee MaluendaJonathan ColombetMaxime BisseuxViviane RavetAnisha DayaramDaisy StaintonSimona KrabergerPeyman Zawar-RezaSharyn GoldstienJames V. BriskieRobyn WhiteHelen TaylorChristopher GomezDavid G. AinleyJon S. HardingRafaela S. FonteneleJoshua SchreckSimone G. RibeiroStephen A. OswaldJennifer M. ArnoldFrançois EnaultArvind VarsaniKenneth M. StedmanAmerican Society for MicrobiologyarticlecrucivirusCRESS-DNA virusesgene transferrecombinationvirus evolutionenvironmental virologyMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020) |
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DOAJ |
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DOAJ |
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EN |
| topic |
crucivirus CRESS-DNA viruses gene transfer recombination virus evolution environmental virology Microbiology QR1-502 |
| spellingShingle |
crucivirus CRESS-DNA viruses gene transfer recombination virus evolution environmental virology Microbiology QR1-502 Ignacio de la Higuera George W. Kasun Ellis L. Torrance Alyssa A. Pratt Amberlee Maluenda Jonathan Colombet Maxime Bisseux Viviane Ravet Anisha Dayaram Daisy Stainton Simona Kraberger Peyman Zawar-Reza Sharyn Goldstien James V. Briskie Robyn White Helen Taylor Christopher Gomez David G. Ainley Jon S. Harding Rafaela S. Fontenele Joshua Schreck Simone G. Ribeiro Stephen A. Oswald Jennifer M. Arnold François Enault Arvind Varsani Kenneth M. Stedman Unveiling Crucivirus Diversity by Mining Metagenomic Data |
| description |
ABSTRACT The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viruses that encode capsid proteins that are most closely related to those encoded by RNA viruses in the family Tombusviridae. The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of capsid genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and 10 capsid-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode. Most of the variation is reflected in the replication-associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins and that the exchange of Rep protein domains between cruciviruses is rarer than intergenic recombination. Additionally, we suggest members of the stramenopiles/alveolates/Rhizaria supergroup as possible crucivirus hosts. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses. IMPORTANCE Viruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Circular Rep-encoding single-stranded (CRESS) DNA viruses are ubiquitous in nature, many are agriculturally important, and they appear to have multiple origins from prokaryotic plasmids. A subset of CRESS-DNA viruses, the cruciviruses, have homologues of capsid proteins encoded by RNA viruses. The genetic structure of cruciviruses attests to the transfer of capsid genes between disparate groups of viruses. However, the evolutionary history of cruciviruses is still unclear. By collecting and analyzing cruciviral sequence data, we provide a deeper insight into the evolutionary intricacies of cruciviruses. Our results reveal an unexpected diversity of this virus group, with frequent recombination as an important determinant of variability. |
| format |
article |
| author |
Ignacio de la Higuera George W. Kasun Ellis L. Torrance Alyssa A. Pratt Amberlee Maluenda Jonathan Colombet Maxime Bisseux Viviane Ravet Anisha Dayaram Daisy Stainton Simona Kraberger Peyman Zawar-Reza Sharyn Goldstien James V. Briskie Robyn White Helen Taylor Christopher Gomez David G. Ainley Jon S. Harding Rafaela S. Fontenele Joshua Schreck Simone G. Ribeiro Stephen A. Oswald Jennifer M. Arnold François Enault Arvind Varsani Kenneth M. Stedman |
| author_facet |
Ignacio de la Higuera George W. Kasun Ellis L. Torrance Alyssa A. Pratt Amberlee Maluenda Jonathan Colombet Maxime Bisseux Viviane Ravet Anisha Dayaram Daisy Stainton Simona Kraberger Peyman Zawar-Reza Sharyn Goldstien James V. Briskie Robyn White Helen Taylor Christopher Gomez David G. Ainley Jon S. Harding Rafaela S. Fontenele Joshua Schreck Simone G. Ribeiro Stephen A. Oswald Jennifer M. Arnold François Enault Arvind Varsani Kenneth M. Stedman |
| author_sort |
Ignacio de la Higuera |
| title |
Unveiling Crucivirus Diversity by Mining Metagenomic Data |
| title_short |
Unveiling Crucivirus Diversity by Mining Metagenomic Data |
| title_full |
Unveiling Crucivirus Diversity by Mining Metagenomic Data |
| title_fullStr |
Unveiling Crucivirus Diversity by Mining Metagenomic Data |
| title_full_unstemmed |
Unveiling Crucivirus Diversity by Mining Metagenomic Data |
| title_sort |
unveiling crucivirus diversity by mining metagenomic data |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/c83420450bfa44719ee6e8cbfc278d91 |
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