Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Jérémy Gauthier; Hélène Boulain; Joke J. F. A. van Vugt; Lyam Baudry; Emma Persyn; Jean-Marc Aury; Benjamin Noel; Anthony Bretaudeau; Fabrice Legeai; Sven Warris; Mohamed A Chebbi; Géraldine Dubreuil; Bernard Duvic; Natacha Kremer; Philippe Gayral; Karine Musset; Thibaut Josse; Diane Bigot; Christophe Bressac; Sébastien Moreau; Georges Periquet; Myriam Harry; Nicolas Montagné; Isabelle Boulogne; Mahnaz Sabeti-Azad; Martine Maïbèche; Thomas Chertemps; Frédérique Hilliou; David Siaussat; Joëlle Amselem; Isabelle Luyten; Claire Capdevielle-Dulac; Karine Labadie; Bruna Laís Merlin; Valérie Barbe; Jetske G de Boer; Martial Marbouty; Fernando Luis Cônsoli; Stéphane Dupas; Aurélie Hua-Van; Gaelle Le Goff; Annie Bézier; Emmanuelle Jacquin-Joly; James B Whitfield; Louise E.M. Vet; Hans M Smid; Laure Kaiser; Romain Koszul; Elisabeth Huguet; Elisabeth A Herniou; Jean-Michel Drezen

doi:10.1038/s42003-020-01623-8

Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Jérémy Gauthier, Hélène Boulain, Joke J. F. A. van Vugt, Lyam Baudry, Emma Persyn, Jean-Marc Aury, Benjamin Noel, Anthony Bretaudeau, Fabrice Legeai, Sven Warris, Mohamed A Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, Philippe Gayral, Karine Musset, Thibaut Josse, Diane Bigot, Christophe Bressac, Sébastien MoreauGeorges Periquet, Myriam Harry, Nicolas Montagné, Isabelle Boulogne, Mahnaz Sabeti-Azad, Martine Maïbèche, Thomas Chertemps, Frédérique Hilliou, David Siaussat, Joëlle Amselem, Isabelle Luyten, Claire Capdevielle-Dulac, Karine Labadie, Bruna Laís Merlin, Valérie Barbe, Jetske G de Boer, Martial Marbouty, Fernando Luis Cônsoli, Stéphane Dupas, Aurélie Hua-Van, Gaelle Le Goff, Annie Bézier, Emmanuelle Jacquin-Joly, James B Whitfield, Louise E.M. Vet, Hans M Smid, Laure Kaiser, Romain Koszul, Elisabeth Huguet, Elisabeth A Herniou, Jean-Michel Drezen (Corresponding author)

NIOO - Terrestrial Ecology (TE)

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Abstract

Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

Original language	English
Pages (from-to)	104
Journal	Communications Biology
Volume	4
Issue number	1
DOIs	https://doi.org/10.1038/s42003-020-01623-8
Publication status	Published - 22 Jan 2021

Keywords

international
Plan_S-Compliant-OA

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10.1038/s42003-020-01623-8Licence: CC BY

7146_GauthierFinal published version, 3.04 MBLicence: CC BY

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Gauthier, J., Boulain, H., van Vugt, J. J. F. A., Baudry, L., Persyn, E., Aury, J.-M., Noel, B., Bretaudeau, A., Legeai, F., Warris, S., Chebbi, M. A., Dubreuil, G., Duvic, B., Kremer, N., Gayral, P., Musset, K., Josse, T., Bigot, D., Bressac, C., ... Drezen, J.-M. (2021). Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization. Communications Biology, 4(1), 104. https://doi.org/10.1038/s42003-020-01623-8

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abstract = "Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.",

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year = "2021",

month = jan,

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doi = "10.1038/s42003-020-01623-8",

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pages = "104",

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Gauthier, J, Boulain, H, van Vugt, JJFA, Baudry, L, Persyn, E, Aury, J-M, Noel, B, Bretaudeau, A, Legeai, F, Warris, S, Chebbi, MA, Dubreuil, G, Duvic, B, Kremer, N, Gayral, P, Musset, K, Josse, T, Bigot, D, Bressac, C, Moreau, S, Periquet, G, Harry, M, Montagné, N, Boulogne, I, Sabeti-Azad, M, Maïbèche, M, Chertemps, T, Hilliou, F, Siaussat, D, Amselem, J, Luyten, I, Capdevielle-Dulac, C, Labadie, K, Merlin, BL, Barbe, V, de Boer, JG, Marbouty, M, Cônsoli, FL, Dupas, S, Hua-Van, A, Le Goff, G, Bézier, A, Jacquin-Joly, E, Whitfield, JB, Vet, LEM, Smid, HM, Kaiser, L, Koszul, R, Huguet, E, Herniou, EA & Drezen, J-M 2021, 'Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization', Communications Biology, vol. 4, no. 1, pp. 104. https://doi.org/10.1038/s42003-020-01623-8

TY - JOUR

T1 - Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

AU - Gauthier, Jérémy

AU - Boulain, Hélène

AU - van Vugt, Joke J. F. A.

AU - Baudry, Lyam

AU - Persyn, Emma

AU - Aury, Jean-Marc

AU - Noel, Benjamin

AU - Bretaudeau, Anthony

AU - Legeai, Fabrice

AU - Warris, Sven

AU - Chebbi, Mohamed A

AU - Dubreuil, Géraldine

AU - Duvic, Bernard

AU - Kremer, Natacha

AU - Gayral, Philippe

AU - Musset, Karine

AU - Josse, Thibaut

AU - Bigot, Diane

AU - Bressac, Christophe

AU - Moreau, Sébastien

AU - Periquet, Georges

AU - Harry, Myriam

AU - Montagné, Nicolas

AU - Boulogne, Isabelle

AU - Sabeti-Azad, Mahnaz

AU - Maïbèche, Martine

AU - Chertemps, Thomas

AU - Hilliou, Frédérique

AU - Siaussat, David

AU - Amselem, Joëlle

AU - Luyten, Isabelle

AU - Capdevielle-Dulac, Claire

AU - Labadie, Karine

AU - Merlin, Bruna Laís

AU - Barbe, Valérie

AU - de Boer, Jetske G

AU - Marbouty, Martial

AU - Cônsoli, Fernando Luis

AU - Dupas, Stéphane

AU - Hua-Van, Aurélie

AU - Le Goff, Gaelle

AU - Bézier, Annie

AU - Jacquin-Joly, Emmanuelle

AU - Whitfield, James B

AU - Vet, Louise E.M.

AU - Smid, Hans M

AU - Kaiser, Laure

AU - Koszul, Romain

AU - Huguet, Elisabeth

AU - Herniou, Elisabeth A

AU - Drezen, Jean-Michel

N1 - 7146, TE; Data archiving: no NIOO data

PY - 2021/1/22

Y1 - 2021/1/22

N2 - Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

AB - Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

KW - international

KW - Plan_S-Compliant-OA

U2 - 10.1038/s42003-020-01623-8

DO - 10.1038/s42003-020-01623-8

M3 - Article

C2 - 33483589

SN - 2399-3642

VL - 4

SP - 104

JO - Communications Biology

JF - Communications Biology

IS - 1

ER -

Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

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