Section: Infections
Topic: Biology of interactions, Microbiology, Evolution

Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)

10.24072/pcjournal.154 - Peer Community Journal, Volume 2 (2022), article no. e44.

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Structural variations (SVs) constitute a significant source of genetic variability in virus genomes. Yet knowledge about SV variability and contribution to the evolutionary process in large double-stranded (ds)DNA viruses is limited. Cyprinid herpesvirus 3 (CyHV-3), also commonly known as koi herpesvirus (KHV), has the largest dsDNA genome within herpesviruses. This virus has become one of the biggest threats to common carp and koi farming, resulting in high morbidity and mortalities of fishes, serious environmental damage, and severe economic losses. A previous study analyzing CyHV-3 virulence evolution during serial passages onto carp cell cultures suggested that CyHV-3 evolves, at least in vitro, through an assembly of haplotypes that alternatively become dominant or under-represented. The present study investigates the SV diversity and dynamics in CyHV-3 genome during 99 serial passages in cell culture using, for the first time, ultra-deep whole-genome and amplicon-based sequencing. The results indicate that KHV polymorphism mostly involves SVs. These SVs display a wide distribution along the genome and exhibit high turnover dynamics with a clear bias towards inversion and deletion events. Analysis of the pathogenesis-associated ORF150 region in ten intermediate cell passages highlighted mainly deletion, inversion and insertion variations that deeply altered the structure of ORF150. Our findings indicate that SV turnovers and defective genomes represent key drivers in the viral population dynamics and in vitro evolution of KHV. Thus, the present study can contribute to the basic research needed to design safe live-attenuated vaccines, classically obtained by viral attenuation after serial passages in cell culture. 

Published online:
DOI: 10.24072/pcjournal.154
Type: Research article
Fuandila, Nurul Novelia 1; Gosselin-Grenet, Anne-Sophie 2; Tilak, Marie-Ka 1; Bergmann, Sven M 3; Escoubas, Jean-Michel 4; Klafack, Sandro 5; Lusiastuti, Angela Mariana 6; Yuhana, Munti 7; Fiston-Lavier, Anna-Sophie 8; Avarre, Jean-Christophe 1; Cherif, Emira 1

1 ISEM, Univ Montpellier, CNRS, IRD, Montpellier, France
2 DGIMI, Univ Montpellier, INRAE, Montpellier, France
3 Institute of Infectology, Friedrich-Loeffer-Institut, Federal Research Institute for Animal Health, Greifswald-Insel Riems, Germany
4 IHPE, Univ Montpellier, CNRS, Ifremer, UPVD, Montpellier, France
5 Department of Experimental Animal Facilities and Biorisk Management, Friedrich-Loeffer-Institut, Federal Research Institute for Animal Health, Greifswald-Insel Riems, Germany
6 Fish Health Laboratory, Research Institute for Freshwater Aquaculture and Fisheries Extension, Bogor, Indonesia
7 Faculty of Fisheries and Marine Sciences, Bogor Agricultural University, Indonesia
8 Institut Universitaire de France (IUF), Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Fuandila, Nurul Novelia and Gosselin-Grenet, Anne-Sophie and Tilak, Marie-Ka and Bergmann, Sven M and Escoubas, Jean-Michel and Klafack, Sandro and Lusiastuti, Angela Mariana and Yuhana, Munti and Fiston-Lavier, Anna-Sophie and Avarre, Jean-Christophe and Cherif, Emira},
     title = {Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded {DNA} koi herpesvirus {(KHV)}},
     journal = {Peer Community Journal},
     eid = {e44},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.154},
     url = {}
AU  - Fuandila, Nurul Novelia
AU  - Gosselin-Grenet, Anne-Sophie
AU  - Tilak, Marie-Ka
AU  - Bergmann, Sven M
AU  - Escoubas, Jean-Michel
AU  - Klafack, Sandro
AU  - Lusiastuti, Angela Mariana
AU  - Yuhana, Munti
AU  - Fiston-Lavier, Anna-Sophie
AU  - Avarre, Jean-Christophe
AU  - Cherif, Emira
TI  - Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)
JO  - Peer Community Journal
PY  - 2022
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PB  - Peer Community In
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DO  - 10.24072/pcjournal.154
ID  - 10_24072_pcjournal_154
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%A Fuandila, Nurul Novelia
%A Gosselin-Grenet, Anne-Sophie
%A Tilak, Marie-Ka
%A Bergmann, Sven M
%A Escoubas, Jean-Michel
%A Klafack, Sandro
%A Lusiastuti, Angela Mariana
%A Yuhana, Munti
%A Fiston-Lavier, Anna-Sophie
%A Avarre, Jean-Christophe
%A Cherif, Emira
%T Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.154
%F 10_24072_pcjournal_154
Fuandila, Nurul Novelia; Gosselin-Grenet, Anne-Sophie; Tilak, Marie-Ka; Bergmann, Sven M; Escoubas, Jean-Michel; Klafack, Sandro; Lusiastuti, Angela Mariana; Yuhana, Munti; Fiston-Lavier, Anna-Sophie; Avarre, Jean-Christophe; Cherif, Emira. Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV). Peer Community Journal, Volume 2 (2022), article  no. e44. doi : 10.24072/pcjournal.154.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.infections.100001

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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