Redondovirus Diversity and Evolution on Global, Individual, and Molecular Scales
is a newly established family of circular Rep-encoding single-stranded (CRESS) DNA viruses found in the human ororespiratory tract. Redondoviruses were previously found in ∼15% of respiratory specimens from U.S. urban subjects; levels were elevated in individuals with periodontitis or critical illne...
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| Published in: | Journal of virology Vol. 95; no. 21; p. e0081721 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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| ISSN: | 1098-5514, 1098-5514 |
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| Abstract | is a newly established family of circular Rep-encoding single-stranded (CRESS) DNA viruses found in the human ororespiratory tract. Redondoviruses were previously found in ∼15% of respiratory specimens from U.S. urban subjects; levels were elevated in individuals with periodontitis or critical illness. Here, we report higher redondovirus prevalence in saliva samples: four rural African populations showed 61 to 82% prevalence, and an urban U.S. population showed 32% prevalence. Longitudinal, limiting-dilution single-genome sequencing revealed diverse strains of both redondovirus species (
and
) in single individuals, persistence over time, and evidence of intergenomic recombination. Computational analysis of viral genomes identified a recombination hot spot associated with a conserved potential DNA stem-loop structure. To assess the possible role of this site in recombination, we carried out
studies which showed that this potential stem-loop was cleaved by the virus-encoded Rep protein. In addition, in reconstructed reactions, a Rep-DNA covalent intermediate was shown to mediate DNA strand transfer at this site. Thus, redondoviruses are highly prevalent in humans, found in individuals on multiple continents, heterogeneous even within individuals and encode a Rep protein implicated in facilitating recombination.
is a recently established family of DNA viruses predominantly found in the human respiratory tract and associated with multiple clinical conditions. In this study, we found high redondovirus prevalence in saliva from urban North American individuals and nonindustrialized African populations in Botswana, Cameroon, Ethiopia, and Tanzania. Individuals on both continents harbored both known redondovirus species. Global prevalence of both species suggests that redondoviruses have long been associated with humans but have remained undetected until recently due to their divergent genomes. By sequencing single redondovirus genomes in longitudinally sampled humans, we found that redondoviruses persisted over time within subjects and likely evolve by recombination. The Rep protein encoded by redondoviruses catalyzes multiple reactions
, consistent with a role in mediating DNA replication and recombination. In summary, we identify high redondovirus prevalence in humans across multiple continents, longitudinal heterogeneity and persistence, and potential mechanisms of redondovirus evolution by recombination. |
|---|---|
| AbstractList | is a newly established family of circular Rep-encoding single-stranded (CRESS) DNA viruses found in the human ororespiratory tract. Redondoviruses were previously found in ∼15% of respiratory specimens from U.S. urban subjects; levels were elevated in individuals with periodontitis or critical illness. Here, we report higher redondovirus prevalence in saliva samples: four rural African populations showed 61 to 82% prevalence, and an urban U.S. population showed 32% prevalence. Longitudinal, limiting-dilution single-genome sequencing revealed diverse strains of both redondovirus species (
and
) in single individuals, persistence over time, and evidence of intergenomic recombination. Computational analysis of viral genomes identified a recombination hot spot associated with a conserved potential DNA stem-loop structure. To assess the possible role of this site in recombination, we carried out
studies which showed that this potential stem-loop was cleaved by the virus-encoded Rep protein. In addition, in reconstructed reactions, a Rep-DNA covalent intermediate was shown to mediate DNA strand transfer at this site. Thus, redondoviruses are highly prevalent in humans, found in individuals on multiple continents, heterogeneous even within individuals and encode a Rep protein implicated in facilitating recombination.
is a recently established family of DNA viruses predominantly found in the human respiratory tract and associated with multiple clinical conditions. In this study, we found high redondovirus prevalence in saliva from urban North American individuals and nonindustrialized African populations in Botswana, Cameroon, Ethiopia, and Tanzania. Individuals on both continents harbored both known redondovirus species. Global prevalence of both species suggests that redondoviruses have long been associated with humans but have remained undetected until recently due to their divergent genomes. By sequencing single redondovirus genomes in longitudinally sampled humans, we found that redondoviruses persisted over time within subjects and likely evolve by recombination. The Rep protein encoded by redondoviruses catalyzes multiple reactions
, consistent with a role in mediating DNA replication and recombination. In summary, we identify high redondovirus prevalence in humans across multiple continents, longitudinal heterogeneity and persistence, and potential mechanisms of redondovirus evolution by recombination. Redondoviridae is a newly established family of circular Rep-encoding single-stranded (CRESS) DNA viruses found in the human ororespiratory tract. Redondoviruses were previously found in ∼15% of respiratory specimens from U.S. urban subjects; levels were elevated in individuals with periodontitis or critical illness. Here, we report higher redondovirus prevalence in saliva samples: four rural African populations showed 61 to 82% prevalence, and an urban U.S. population showed 32% prevalence. Longitudinal, limiting-dilution single-genome sequencing revealed diverse strains of both redondovirus species (Brisavirus and Vientovirus) in single individuals, persistence over time, and evidence of intergenomic recombination. Computational analysis of viral genomes identified a recombination hot spot associated with a conserved potential DNA stem-loop structure. To assess the possible role of this site in recombination, we carried out in vitro studies which showed that this potential stem-loop was cleaved by the virus-encoded Rep protein. In addition, in reconstructed reactions, a Rep-DNA covalent intermediate was shown to mediate DNA strand transfer at this site. Thus, redondoviruses are highly prevalent in humans, found in individuals on multiple continents, heterogeneous even within individuals and encode a Rep protein implicated in facilitating recombination. IMPORTANCERedondoviridae is a recently established family of DNA viruses predominantly found in the human respiratory tract and associated with multiple clinical conditions. In this study, we found high redondovirus prevalence in saliva from urban North American individuals and nonindustrialized African populations in Botswana, Cameroon, Ethiopia, and Tanzania. Individuals on both continents harbored both known redondovirus species. Global prevalence of both species suggests that redondoviruses have long been associated with humans but have remained undetected until recently due to their divergent genomes. By sequencing single redondovirus genomes in longitudinally sampled humans, we found that redondoviruses persisted over time within subjects and likely evolve by recombination. The Rep protein encoded by redondoviruses catalyzes multiple reactions in vitro, consistent with a role in mediating DNA replication and recombination. In summary, we identify high redondovirus prevalence in humans across multiple continents, longitudinal heterogeneity and persistence, and potential mechanisms of redondovirus evolution by recombination.Redondoviridae is a newly established family of circular Rep-encoding single-stranded (CRESS) DNA viruses found in the human ororespiratory tract. Redondoviruses were previously found in ∼15% of respiratory specimens from U.S. urban subjects; levels were elevated in individuals with periodontitis or critical illness. Here, we report higher redondovirus prevalence in saliva samples: four rural African populations showed 61 to 82% prevalence, and an urban U.S. population showed 32% prevalence. Longitudinal, limiting-dilution single-genome sequencing revealed diverse strains of both redondovirus species (Brisavirus and Vientovirus) in single individuals, persistence over time, and evidence of intergenomic recombination. Computational analysis of viral genomes identified a recombination hot spot associated with a conserved potential DNA stem-loop structure. To assess the possible role of this site in recombination, we carried out in vitro studies which showed that this potential stem-loop was cleaved by the virus-encoded Rep protein. In addition, in reconstructed reactions, a Rep-DNA covalent intermediate was shown to mediate DNA strand transfer at this site. Thus, redondoviruses are highly prevalent in humans, found in individuals on multiple continents, heterogeneous even within individuals and encode a Rep protein implicated in facilitating recombination. IMPORTANCERedondoviridae is a recently established family of DNA viruses predominantly found in the human respiratory tract and associated with multiple clinical conditions. In this study, we found high redondovirus prevalence in saliva from urban North American individuals and nonindustrialized African populations in Botswana, Cameroon, Ethiopia, and Tanzania. Individuals on both continents harbored both known redondovirus species. Global prevalence of both species suggests that redondoviruses have long been associated with humans but have remained undetected until recently due to their divergent genomes. By sequencing single redondovirus genomes in longitudinally sampled humans, we found that redondoviruses persisted over time within subjects and likely evolve by recombination. The Rep protein encoded by redondoviruses catalyzes multiple reactions in vitro, consistent with a role in mediating DNA replication and recombination. In summary, we identify high redondovirus prevalence in humans across multiple continents, longitudinal heterogeneity and persistence, and potential mechanisms of redondovirus evolution by recombination. |
| Author | Allen, Audrey A Ranciaro, Alessia Woldemeskel, Dawit Collman, Ronald G Nyambo, Thomas Khatib, Layla A Mokone, Gaonyadiwe G Mpoloka, Sununguko Wata Dothard, Marisol I Bushman, Frederic D Belay, Gurja Fokunang, Charles Fitzgerald, Ayannah S Thompson, Simon R Hwang, Young Graham-Wooten, Jevon Beggs, William R Njamnshi, Alfred K Mbunwe, Eric Tishkoff, Sarah A Taylor, Louis J Rubel, Meagan A Campbell, Michael C Roche, Aoife M |
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Young organization: Department of Microbiology, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 6 givenname: Aoife M surname: Roche fullname: Roche, Aoife M organization: Department of Microbiology, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 7 givenname: Jevon surname: Graham-Wooten fullname: Graham-Wooten, Jevon organization: Department of Medicine, Pulmonary, Allergy and Critical Care Division, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 8 givenname: Ayannah S surname: Fitzgerald fullname: Fitzgerald, Ayannah S organization: Department of Medicine, Pulmonary, Allergy and Critical Care Division, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 9 givenname: Layla A surname: Khatib fullname: Khatib, Layla A organization: Department of Medicine, Pulmonary, Allergy and Critical Care Division, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 10 givenname: Alessia surname: Ranciaro fullname: Ranciaro, Alessia organization: Department of Genetics, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 11 givenname: Simon R surname: Thompson fullname: Thompson, Simon R organization: Department of Genetics, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 12 givenname: William R surname: Beggs fullname: Beggs, William R organization: Department of Genetics, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 13 givenname: Michael C surname: Campbell fullname: Campbell, Michael C organization: Department of Genetics, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 14 givenname: Gaonyadiwe G surname: Mokone fullname: Mokone, Gaonyadiwe G organization: University of Botswanagrid.7621.2, Faculty of Medicine, Gaborone, Botswana – sequence: 15 givenname: Sununguko Wata surname: Mpoloka fullname: Mpoloka, Sununguko Wata organization: University of Botswanagrid.7621.2, Biological Sciences, Gaborone, Botswana – sequence: 16 givenname: Charles surname: Fokunang fullname: Fokunang, Charles organization: Department of Pharmacotoxicology and Pharmacokinetics, Faculty of Medicine and Biomedical Sciences, The University of Yaoundé I, Yaoundé, Cameroon – sequence: 17 givenname: Alfred K surname: Njamnshi fullname: Njamnshi, Alfred K organization: Brain Research Africa Initiative, Neuroscience Lab, Faculty of Medicine and Biomedical Sciences, The University of Yaoundé I, Yaoundé, Cameroon – sequence: 18 givenname: Eric surname: Mbunwe fullname: Mbunwe, Eric organization: Department of Genetics, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 19 givenname: Dawit surname: Woldemeskel fullname: Woldemeskel, Dawit organization: Addis Ababa Universitygrid.7123.7, Department of Microbial Cellular and Molecular Biology, Addis Ababa, Ethiopia – sequence: 20 givenname: Gurja surname: Belay fullname: Belay, Gurja organization: Addis Ababa Universitygrid.7123.7, Department of Microbial Cellular and Molecular Biology, Addis Ababa, Ethiopia – sequence: 21 givenname: Thomas surname: Nyambo fullname: Nyambo, Thomas organization: Kampala International Universitygrid.440478.b in Tanzania, Dar es Salaam, Tanzania – sequence: 22 givenname: Sarah A surname: Tishkoff fullname: Tishkoff, Sarah A organization: Department of Biology, School of Arts and Sciences, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 23 givenname: Ronald G orcidid: 0000-0002-0508-3701 surname: Collman fullname: Collman, Ronald G organization: Department of Medicine, Pulmonary, Allergy and Critical Care Division, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA – sequence: 24 givenname: Frederic D orcidid: 0000-0003-4740-4056 surname: Bushman fullname: Bushman, Frederic D organization: Department of Microbiology, Perelman School of Medicine, University of Pennsylvaniagrid.25879.31, Philadelphia, Pennsylvania, USA |
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| SubjectTerms | Africa - epidemiology Biodiversity Critical Illness DNA Virus Infections - epidemiology DNA Virus Infections - virology DNA Viruses - classification DNA Viruses - genetics DNA Viruses - metabolism DNA-Binding Proteins - metabolism Evolution, Molecular Genome, Viral Humans Metagenomics Mouth - virology Periodontitis - virology Phylogeny Prevalence Respiratory System - virology Rural Population Saliva - virology United States - epidemiology Viral Proteins - metabolism |
| Title | Redondovirus Diversity and Evolution on Global, Individual, and Molecular Scales |
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