Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology

Chapparvoviruses (ChPVs) comprise a divergent lineage of the <i>Parvoviridae</i> ssDNA virus family and evolved to infect vertebrate animals independently from the <i>Parvovirinae</i> subfamily. Despite being pathogenic and widespread in environmental samples and metagenomic...

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Main Authors: Judit J. Penzes, Jason T. Kaelber
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Viruses
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Online Access:https://www.mdpi.com/1999-4915/17/5/679
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author Judit J. Penzes
Jason T. Kaelber
author_facet Judit J. Penzes
Jason T. Kaelber
author_sort Judit J. Penzes
collection DOAJ
description Chapparvoviruses (ChPVs) comprise a divergent lineage of the <i>Parvoviridae</i> ssDNA virus family and evolved to infect vertebrate animals independently from the <i>Parvovirinae</i> subfamily. Despite being pathogenic and widespread in environmental samples and metagenomic assemblies, their structural characterization has proven challenging. Here, we report the first structural analysis of a ChPV, represented by the fish pathogen, Syngnathus scovelli chapparvovirus (SsChPV). We show through the SsChPV structure that the lineage harbors a surface morphology, subunit structure, and multimer interactions that are unique among parvoviruses. The SsChPV capsid evolved a threefold-related depression of α-helices that is analogous to the β-annulus pore of denso- and hamaparvoviruses and may play a role in monomer oligomerization during assembly. As interacting β-strands are absent from the twofold symmetry axis, the viral particle lacks the typical stability and resilience of parvovirus capsids. Although all parvoviruses thus far rely on the threading of large, flexible N-terminal domains to the capsid surface for their intracellular trafficking, our results show that ChPVs completely lack any such N-terminal sequences. This led to the subsequent degradation of their fivefold channel, the site of N-terminus externalization. These findings suggest that ChPVs harbor an infectious pathway that significantly deviates from the rest of the <i>Parvoviridae</i>.
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spelling doaj-art-e93a4525bd9b42478a179aa45dc4dc182025-08-20T02:34:02ZengMDPI AGViruses1999-49152025-05-0117567910.3390/v17050679Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural BiologyJudit J. Penzes0Jason T. Kaelber1Institute for Quantitative Biomedicine, Rutgers, The State University of New Jersey, Piscataway, NJ 08812, USAInstitute for Quantitative Biomedicine, Rutgers, The State University of New Jersey, Piscataway, NJ 08812, USAChapparvoviruses (ChPVs) comprise a divergent lineage of the <i>Parvoviridae</i> ssDNA virus family and evolved to infect vertebrate animals independently from the <i>Parvovirinae</i> subfamily. Despite being pathogenic and widespread in environmental samples and metagenomic assemblies, their structural characterization has proven challenging. Here, we report the first structural analysis of a ChPV, represented by the fish pathogen, Syngnathus scovelli chapparvovirus (SsChPV). We show through the SsChPV structure that the lineage harbors a surface morphology, subunit structure, and multimer interactions that are unique among parvoviruses. The SsChPV capsid evolved a threefold-related depression of α-helices that is analogous to the β-annulus pore of denso- and hamaparvoviruses and may play a role in monomer oligomerization during assembly. As interacting β-strands are absent from the twofold symmetry axis, the viral particle lacks the typical stability and resilience of parvovirus capsids. Although all parvoviruses thus far rely on the threading of large, flexible N-terminal domains to the capsid surface for their intracellular trafficking, our results show that ChPVs completely lack any such N-terminal sequences. This led to the subsequent degradation of their fivefold channel, the site of N-terminus externalization. These findings suggest that ChPVs harbor an infectious pathway that significantly deviates from the rest of the <i>Parvoviridae</i>.https://www.mdpi.com/1999-4915/17/5/679cryo-EMparvovirusvirus structurevirus evolutionfish pathogencapsid structure
spellingShingle Judit J. Penzes
Jason T. Kaelber
Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology
Viruses
cryo-EM
parvovirus
virus structure
virus evolution
fish pathogen
capsid structure
title Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology
title_full Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology
title_fullStr Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology
title_full_unstemmed Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology
title_short Capsid Structure of the Fish Pathogen Syngnathus Scovelli Chapparvovirus Offers a New Perspective on Parvovirus Structural Biology
title_sort capsid structure of the fish pathogen syngnathus scovelli chapparvovirus offers a new perspective on parvovirus structural biology
topic cryo-EM
parvovirus
virus structure
virus evolution
fish pathogen
capsid structure
url https://www.mdpi.com/1999-4915/17/5/679
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