Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

J. Gauthier; H. Boulain; J.F.A. van Vugt; L. Baudry; E. Persyn; J.M. Aury; B. Noel; A. Bretaudeau; Fabrice Legeai; S. Warris; M. Amine Chebbi; Géraldine Dubreuil; Bernard Duvic; Natacha Kremer; P. Gayral; K. Musset; J. Thibaut; D. Bigot; C. Bressac; S. Moreau; G. Periquet; M. Harry; N. Montagné; I. Boulogne; M. Sabeti-Azad; M. Maïbèche; T. Chertemps; F. Hilliou; D. Siaussat; J. Amselem; I. Luyten; C. Capdevielle-Dulac; Karine Labadie; B. Laís Merlin; Valérie Barbe; J.G. de Boer; M. Marbouty; F.L. Cônsoli; S. Dupas; A. Hua Van; G. Le Goff; Annie Bézier; E. Jacquin-Joly; James B. Whitfield; L.E.M. Vet; H.M. Smid; L. Kaiser-Arnault; R. Koszul; Elisabeth Huguet; Elisabeth A. Herniou; J.M. Drezen

doi:10.1101/2020.03.19.994459

Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

J. Gauthier, H. Boulain, J.F.A. van Vugt, L. Baudry, E. Persyn, J.M. Aury, B. Noel, A. Bretaudeau, Fabrice Legeai, S. Warris, M. Amine Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, P. Gayral, K. Musset, J. Thibaut, D. Bigot, C. Bressac, S. MoreauG. Periquet, M. Harry, N. Montagné, I. Boulogne, M. Sabeti-Azad, M. Maïbèche, T. Chertemps, F. Hilliou, D. Siaussat, J. Amselem, I. Luyten, C. Capdevielle-Dulac, Karine Labadie, B. Laís Merlin, Valérie Barbe, J.G. de Boer, M. Marbouty, F.L. Cônsoli, S. Dupas, A. Hua Van, G. Le Goff, Annie Bézier, E. Jacquin-Joly, James B. Whitfield, L.E.M. Vet, H.M. Smid, L. Kaiser-Arnault, R. Koszul, Elisabeth Huguet, Elisabeth A. Herniou, J.M. Drezen

Research output: Working paper › Academic

Abstract

Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.

Original language	English
Publisher	BioRxiv
DOIs	https://doi.org/10.1101/2020.03.19.994459
Publication status	Published - 2020

Publication series

Name	Cold Spring Harbor Perspectives in Biology
Publisher	Cold Spring Harbor Laboratory Press
ISSN (Print)	1943-0264

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https://edepot.wur.nl/543143Licence: CC BY-NC-ND

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Gauthier, J., Boulain, H., van Vugt, J. F. A., Baudry, L., Persyn, E., Aury, J. M., Noel, B., Bretaudeau, A., Legeai, F., Warris, S., Amine Chebbi, M., Dubreuil, G., Duvic, B., Kremer, N., Gayral, P., Musset, K., Thibaut, J., Bigot, D., Bressac, C., ... Drezen, J. M. (2020). Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes. (Cold Spring Harbor Perspectives in Biology). BioRxiv. https://doi.org/10.1101/2020.03.19.994459

@techreport{8f86f4d7886d45da86492b23e7b17535,

title = "Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes",

abstract = "Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.",

author = "J. Gauthier and H. Boulain and {van Vugt}, J.F.A. and L. Baudry and E. Persyn and J.M. Aury and B. Noel and A. Bretaudeau and Fabrice Legeai and S. Warris and {Amine Chebbi}, M. and G{\'e}raldine Dubreuil and Bernard Duvic and Natacha Kremer and P. Gayral and K. Musset and J. Thibaut and D. Bigot and C. Bressac and S. Moreau and G. Periquet and M. Harry and N. Montagn{\'e} and I. Boulogne and M. Sabeti-Azad and M. Ma{\"i}b{\`e}che and T. Chertemps and F. Hilliou and D. Siaussat and J. Amselem and I. Luyten and C. Capdevielle-Dulac and Karine Labadie and {La{\'i}s Merlin}, B. and Val{\'e}rie Barbe and {de Boer}, J.G. and M. Marbouty and F.L. C{\^o}nsoli and S. Dupas and {Hua Van}, A. and {Le Goff}, G. and Annie B{\'e}zier and E. Jacquin-Joly and Whitfield, {James B.} and L.E.M. Vet and H.M. Smid and L. Kaiser-Arnault and R. Koszul and Elisabeth Huguet and Herniou, {Elisabeth A.} and J.M. Drezen",

year = "2020",

doi = "10.1101/2020.03.19.994459",

language = "English",

series = "Cold Spring Harbor Perspectives in Biology",

publisher = "BioRxiv",

address = "United States",

type = "WorkingPaper",

institution = "BioRxiv",

}

Gauthier, J, Boulain, H, van Vugt, JFA, Baudry, L, Persyn, E, Aury, JM, Noel, B, Bretaudeau, A, Legeai, F, Warris, S, Amine Chebbi, M, Dubreuil, G, Duvic, B, Kremer, N, Gayral, P, Musset, K, Thibaut, J, 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, Laís Merlin, B, 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-Arnault, L, Koszul, R, Huguet, E, Herniou, EA & Drezen, JM 2020 'Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes' Cold Spring Harbor Perspectives in Biology, BioRxiv. https://doi.org/10.1101/2020.03.19.994459

TY - UNPB

T1 - Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

AU - Gauthier, J.

AU - Boulain, H.

AU - van Vugt, J.F.A.

AU - Baudry, L.

AU - Persyn, E.

AU - Aury, J.M.

AU - Noel, B.

AU - Bretaudeau, A.

AU - Legeai, Fabrice

AU - Warris, S.

AU - Amine Chebbi, M.

AU - Dubreuil, Géraldine

AU - Duvic, Bernard

AU - Kremer, Natacha

AU - Gayral, P.

AU - Musset, K.

AU - Thibaut, J.

AU - Bigot, D.

AU - Bressac, C.

AU - Moreau, S.

AU - Periquet, G.

AU - Harry, M.

AU - Montagné, N.

AU - Boulogne, I.

AU - Sabeti-Azad, M.

AU - Maïbèche, M.

AU - Chertemps, T.

AU - Hilliou, F.

AU - Siaussat, D.

AU - Amselem, J.

AU - Luyten, I.

AU - Capdevielle-Dulac, C.

AU - Labadie, Karine

AU - Laís Merlin, B.

AU - Barbe, Valérie

AU - de Boer, J.G.

AU - Marbouty, M.

AU - Cônsoli, F.L.

AU - Dupas, S.

AU - Hua Van, A.

AU - Le Goff, G.

AU - Bézier, Annie

AU - Jacquin-Joly, E.

AU - Whitfield, James B.

AU - Vet, L.E.M.

AU - Smid, H.M.

AU - Kaiser-Arnault, L.

AU - Koszul, R.

AU - Huguet, Elisabeth

AU - Herniou, Elisabeth A.

AU - Drezen, J.M.

PY - 2020

Y1 - 2020

N2 - Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.

AB - Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.

U2 - 10.1101/2020.03.19.994459

DO - 10.1101/2020.03.19.994459

M3 - Working paper

T3 - Cold Spring Harbor Perspectives in Biology

BT - Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

PB - BioRxiv

ER -

Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

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