An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts

Chapparvoviruses (ChPVs) comprise a divergent, recently identified group of parvoviruses (family <i>Parvoviridae</i>), associated with nephropathy in immunocompromised laboratory mice and with prevalence in deep sequencing results of livestock showing diarrhea. Here, we investigate the b...

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Main Authors: Judit J. Pénzes, William Marciel de Souza, Mavis Agbandje-McKenna, Robert J. Gifford
Format: Article
Language:English
Published: MDPI AG 2019-06-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/11/6/525
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spelling doaj-d23667a911f945909c77d9eb624832602020-11-25T01:14:52ZengMDPI AGViruses1999-49152019-06-0111652510.3390/v11060525v11060525An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate HostsJudit J. Pénzes0William Marciel de Souza1Mavis Agbandje-McKenna2Robert J. Gifford3McKnight Brain Institute and Department of Biochemistry and Molecular Biology, University of Florida, 1149 Newell Dr, Gainesville, FL 32610, USAVirology Research Center, School of Medicine of Ribeirão Preto of the University of São Paulo, Ribeirão Preto, BrazilMcKnight Brain Institute and Department of Biochemistry and Molecular Biology, University of Florida, 1149 Newell Dr, Gainesville, FL 32610, USAMedical Research Council-University of Glasgow Centre for Virus Research, 464 Bearsden Road, Glasgow G61 1QH, UKChapparvoviruses (ChPVs) comprise a divergent, recently identified group of parvoviruses (family <i>Parvoviridae</i>), associated with nephropathy in immunocompromised laboratory mice and with prevalence in deep sequencing results of livestock showing diarrhea. Here, we investigate the biological and evolutionary characteristics of ChPVs via comparative in silico analyses, incorporating sequences derived from endogenous parvoviral elements (EPVs) as well as exogenous parvoviruses. We show that ChPVs are an ancient lineage within the <i>Parvoviridae</i>, clustering separately from members of both currently established subfamilies. Consistent with this, they exhibit a number of characteristic features, including several putative auxiliary protein-encoding genes, and capsid proteins with no sequence-level homology to those of other parvoviruses. Homology modeling indicates the absence of a &#946;-A strand, normally part of the luminal side of the parvoviral capsid protein core. Our findings demonstrate that the ChPV lineage infects an exceptionally broad range of host species, including both vertebrates and invertebrates. Furthermore, we observe that ChPVs found in fish are more closely related to those from invertebrates than they are to those of amniote vertebrates. This suggests that transmission between distantly related host species may have occurred in the past and that the <i>Parvoviridae</i> family can no longer be divided based on host affiliation.https://www.mdpi.com/1999-4915/11/6/525chapparvovirusparvovirus evolutionendogenous viral elements<i>Parvoviridae</i>densovirushomology modelingnew viruses
collection DOAJ
language English
format Article
sources DOAJ
author Judit J. Pénzes
William Marciel de Souza
Mavis Agbandje-McKenna
Robert J. Gifford
spellingShingle Judit J. Pénzes
William Marciel de Souza
Mavis Agbandje-McKenna
Robert J. Gifford
An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts
Viruses
chapparvovirus
parvovirus evolution
endogenous viral elements
<i>Parvoviridae</i>
densovirus
homology modeling
new viruses
author_facet Judit J. Pénzes
William Marciel de Souza
Mavis Agbandje-McKenna
Robert J. Gifford
author_sort Judit J. Pénzes
title An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts
title_short An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts
title_full An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts
title_fullStr An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts
title_full_unstemmed An Ancient Lineage of Highly Divergent Parvoviruses Infects both Vertebrate and Invertebrate Hosts
title_sort ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts
publisher MDPI AG
series Viruses
issn 1999-4915
publishDate 2019-06-01
description Chapparvoviruses (ChPVs) comprise a divergent, recently identified group of parvoviruses (family <i>Parvoviridae</i>), associated with nephropathy in immunocompromised laboratory mice and with prevalence in deep sequencing results of livestock showing diarrhea. Here, we investigate the biological and evolutionary characteristics of ChPVs via comparative in silico analyses, incorporating sequences derived from endogenous parvoviral elements (EPVs) as well as exogenous parvoviruses. We show that ChPVs are an ancient lineage within the <i>Parvoviridae</i>, clustering separately from members of both currently established subfamilies. Consistent with this, they exhibit a number of characteristic features, including several putative auxiliary protein-encoding genes, and capsid proteins with no sequence-level homology to those of other parvoviruses. Homology modeling indicates the absence of a &#946;-A strand, normally part of the luminal side of the parvoviral capsid protein core. Our findings demonstrate that the ChPV lineage infects an exceptionally broad range of host species, including both vertebrates and invertebrates. Furthermore, we observe that ChPVs found in fish are more closely related to those from invertebrates than they are to those of amniote vertebrates. This suggests that transmission between distantly related host species may have occurred in the past and that the <i>Parvoviridae</i> family can no longer be divided based on host affiliation.
topic chapparvovirus
parvovirus evolution
endogenous viral elements
<i>Parvoviridae</i>
densovirus
homology modeling
new viruses
url https://www.mdpi.com/1999-4915/11/6/525
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