A novel and diverse family of filamentous DNA viruses associated with parasitic wasps

Authors: GUINET, BENJAMIN - University Of Lyon; LEOBOLD, MATTHIEU - Institut De Recherche En Sciencies De La Sante; HERNIOU, ELISABETH - Institut De Recherche En Sciencies De La Sante; BLOIN, PIERRICK - Institut De Recherche En Sciencies De La Sante; BURLET, NELLY - University Of Lyon; BREDLAU, JUSTIN - Virginia Commonwealth University; NAVRATIL, VINCENT - University Of Lyon; RAVALLEC, MARC - University Of Lyon; UZBEKOV, RUSTEM - University Of Lyon; KESTER, KAREN - Virginia Commonwealth University; Gundersen-Rindal, Dawn; DREZEN, JEAN-MICHEL - University Of Lyon; VARALDI, JULIEN - University Of Lyon; BEZIER, ANNIE - Institut De Recherche En Sciencies De La Sante

Submitted to: Virus Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/17/2024
Publication Date: 3/2/2024
Citation: Guinet, B., Leobold, M., Herniou, E., Bloin, P., Burlet, N., Bredlau, J., Navratil, V., Ravallec, M., Uzbekov, ., Kester, K., Gundersen, D.E., Drezen, J., Varaldi, J., Bezier, A. 2024. A novel and diverse family of filamentous DNA viruses associated with parasitic wasps. Virus Evolution. 10(1): Article eveae022. https://doi.org/10.1093/ve/veae022.
DOI: https://doi.org/10.1093/ve/veae022

Interpretive Summary: Parasitoid wasps often contain viruses that serve roles, for example in parasitization of various insect hosts. Since the 1970s, filamentous virus particles have been observed by electronic microscopy in several species of parasitoid wasps but until recently, no genomic data was available for these. The current study provided the first comparative morphological and genomic analyses of filamentous viruses associated with a parasitoid wasp. Genomes of six filamentous viruses were newly obtained, and their core genomes were characterized. Evidence showed that these viruses regularly integrated into the genome of numerous insects, mostly Hymenoptera with parasitoid lifestyle, suggesting a specialization of these viruses on these hosts. A new family, Filamentoviridae, was proposed for these viruses. This information will be useful for scientists and those interested in insect biological control and systematics.

Technical Abstract: Large dsDNA viruses from the Naldaviricetes class are currently composed of four viral families infecting insects and/or crustaceans. Since the 1970s, particles described as filamentous viruses have been observed by electronic microscopy in several species of Hymenoptera parasitoids but until recently, no genomic data was available. This study provides the first comparative morphological and genomic analyses of these filamentous viruses. We analyzed the genomes of seven filamentous viruses, six of which were newly obtained, to gain a better understanding of their evolutionary history. We show these filamentous viruses share all genomic features of the Naldaviricetes and that their core genome comprises five specific genes that distinguish them from their closest relatives the hytrosaviruses. By mining public databases, we also provide evidence that these viruses regularly integrated into the genome of numerous insects, mostly Hymenoptera with parasitoid lifestyle, suggesting a specialization of these viruses on these hosts. Finally, we propose a taxonomical revision of the class Naldaviricetes in which filamentous viruses related to the Leptopilina boulardi filamentous virus (LbFV) constitute a fifth family within the order Lefavirales. We propose to name this new family, Filamentoviridae.