Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)

Abstract Background Cotesia congregata is a parasitoid Hymenoptera belonging to the Braconidae family and carrying CCBV (Cotesia congregata Bracovirus), an endosymbiotic polydnavirus. CCBV virus is considered as the main virulence factor of this species, which has raised questions, over the past thi...

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Main Authors: Sébastien J. M. Moreau, Lorène Marchal, Hélène Boulain, Karine Musset, Valérie Labas, Daniel Tomas, Jérémy Gauthier, Jean-Michel Drezen
Format: Article
Language:English
Published: BMC 2025-04-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11604-y
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author Sébastien J. M. Moreau
Lorène Marchal
Hélène Boulain
Karine Musset
Valérie Labas
Daniel Tomas
Jérémy Gauthier
Jean-Michel Drezen
author_facet Sébastien J. M. Moreau
Lorène Marchal
Hélène Boulain
Karine Musset
Valérie Labas
Daniel Tomas
Jérémy Gauthier
Jean-Michel Drezen
author_sort Sébastien J. M. Moreau
collection DOAJ
description Abstract Background Cotesia congregata is a parasitoid Hymenoptera belonging to the Braconidae family and carrying CCBV (Cotesia congregata Bracovirus), an endosymbiotic polydnavirus. CCBV virus is considered as the main virulence factor of this species, which has raised questions, over the past thirty years, about the potential roles of venom in the parasitic interaction between C. congregata and its host, Manduca sexta (Lepidoptera: Sphingidae). To investigate C. congregata venom composition, we identified genes overexpressed in the venom glands (VGs) compared to ovaries, analyzed the protein composition of this fluid and performed a detailed analysis of conserved domains of these proteins. Results Of the 14 140 known genes of the C. congregata genome, 659 genes were significantly over-expressed (with 10-fold or higher changes in expression) in the VGs of female C. congregata, compared with the ovaries. We identified 30 proteins whose presence was confirmed in venom extracts by proteomic analyses. Twenty-four of these were produced as precursor molecules containing a predicted signal peptide. Six of the proteins lacked a predicted signal peptide, suggesting that venom production in C. congregata also involves non-canonical secretion mechanisms. We have also analysed 18 additional proteins and peptides of interest whose presence in venom remains uncertain, but which could play a role in VG function. Conclusions Our results show that the venom of C. congregata not only contains proteins (including several enzymes) homologous to well-known venomous compounds, but also original proteins that appear to be specific to this species. This exhaustive study sheds a new light on this venom composition, the molecular diversity of which was unexpected. These data pave the way for targeted functional analyses and to better understand the evolutionary mechanisms that have led to the formation of the venomous arsenals we observe today in parasitoid insects.
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spelling doaj-art-4f245fbd26f444df91eda8b1d8757beb2025-08-20T03:52:23ZengBMCBMC Genomics1471-21642025-04-0126112010.1186/s12864-025-11604-yMulti-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)Sébastien J. M. Moreau0Lorène Marchal1Hélène Boulain2Karine Musset3Valérie Labas4Daniel Tomas5Jérémy Gauthier6Jean-Michel Drezen7Institut de Recherche sur la Biologie de l’Insecte, UMR 7261 CNRS, Université de ToursInstitut de Recherche sur la Biologie de l’Insecte, UMR 7261 CNRS, Université de ToursDepartment of Ecology and Evolution, University of LausanneInstitut de Recherche sur la Biologie de l’Insecte, UMR 7261 CNRS, Université de ToursPRC, INRAE, CNRS, Université de ToursPRC, INRAE, CNRS, Université de ToursNaturéum - Cantonal Museum of Natural SciencesInstitut de Recherche sur la Biologie de l’Insecte, UMR 7261 CNRS, Université de ToursAbstract Background Cotesia congregata is a parasitoid Hymenoptera belonging to the Braconidae family and carrying CCBV (Cotesia congregata Bracovirus), an endosymbiotic polydnavirus. CCBV virus is considered as the main virulence factor of this species, which has raised questions, over the past thirty years, about the potential roles of venom in the parasitic interaction between C. congregata and its host, Manduca sexta (Lepidoptera: Sphingidae). To investigate C. congregata venom composition, we identified genes overexpressed in the venom glands (VGs) compared to ovaries, analyzed the protein composition of this fluid and performed a detailed analysis of conserved domains of these proteins. Results Of the 14 140 known genes of the C. congregata genome, 659 genes were significantly over-expressed (with 10-fold or higher changes in expression) in the VGs of female C. congregata, compared with the ovaries. We identified 30 proteins whose presence was confirmed in venom extracts by proteomic analyses. Twenty-four of these were produced as precursor molecules containing a predicted signal peptide. Six of the proteins lacked a predicted signal peptide, suggesting that venom production in C. congregata also involves non-canonical secretion mechanisms. We have also analysed 18 additional proteins and peptides of interest whose presence in venom remains uncertain, but which could play a role in VG function. Conclusions Our results show that the venom of C. congregata not only contains proteins (including several enzymes) homologous to well-known venomous compounds, but also original proteins that appear to be specific to this species. This exhaustive study sheds a new light on this venom composition, the molecular diversity of which was unexpected. These data pave the way for targeted functional analyses and to better understand the evolutionary mechanisms that have led to the formation of the venomous arsenals we observe today in parasitoid insects.https://doi.org/10.1186/s12864-025-11604-yCotesia congregataTranscriptomicsProteomics; Braconidae; ParasitoidVenom
spellingShingle Sébastien J. M. Moreau
Lorène Marchal
Hélène Boulain
Karine Musset
Valérie Labas
Daniel Tomas
Jérémy Gauthier
Jean-Michel Drezen
Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)
BMC Genomics
Cotesia congregata
Transcriptomics
Proteomics; Braconidae; Parasitoid
Venom
title Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)
title_full Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)
title_fullStr Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)
title_full_unstemmed Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)
title_short Multi-omic approach to characterize the venom of the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)
title_sort multi omic approach to characterize the venom of the parasitic wasp cotesia congregata hymenoptera braconidae
topic Cotesia congregata
Transcriptomics
Proteomics; Braconidae; Parasitoid
Venom
url https://doi.org/10.1186/s12864-025-11604-y
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