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A virus at home in parasitic wasps

Genoscope was part of an international team that assembled the genome of Cotesia wasps and identified therein chromosomal colonization by a virus that settled into the wasp genome a hundred-million years ago. Their results, published in Communications Biology, suggest that the evolutionary course of a virus integrated within the genome of a eukaryote changes completely when the former is beneficial to the latter.

Published on 14 February 2021

Although it may be difficult to believe with the current health crisis, not all viruses are deleterious to their hosts. Indeed some confer new functions to the organisms they infect. A spectacular example of this is the integration of a bracovirus within the genome of Cotesia genus wasps roughly 100-million years ago during the Cretaceous period. Cotesia species lay their eggs inside of caterpillars, within which the wasp larvae develop. With the eggs, the wasps also produce and inject massive amounts of bracovirus particles in the host caterpillars. Those particles ensure the production of virulence factors that inhibit the immune system and modify the physiology of the caterpillar, thus enabling the development of the wasp larvae in its body.

An international consortium (France¹, Netherlands, Brazil, United States) headed by the Institute for Research on Insect Biology (IRBI - CNRS/University of Tours) has recently shown that bracovirus genes have colonized all of the wasp's chromosomes. Several Genoscope² laboratories were part of the consortium, providing the sequencing and complete assembly of the genomes of various Cotesia species, without which the obtained results would not have been possible. Most viruses integrating a genome will be progressively eliminated over time. The bracovirus within the Cotesia wasp genomes is an exception, having expanded therein to become genetically enormous, with a genome of close to 1 megabase. That makes it comparable in terms of genetic size to some "giant viruses," like the mimiviruses that infect amoebae. The bracovirus genes have dispersed throughout the Cotesia chromosomes. However, the genes specific to viral functions, such as the formation of viral particles or the circular DNA injected into the caterpillars, are concentrated in certain chromosome regions. The largest—comparable in size to the major histocompatibility complex, a gene group essential to mammal immunity—constitutes most of the short arm of chromosome 5. In the international team's study, that regionalized architecture was shown to be highly conserved across the different Cotesia species, suggesting strong evolutionary constraints for its maintenance. Despite the massive production of viral particles, an analysis of the expression of immune-associated genes in the wasp showed that this latter does not consider them to be foreign. Thus after 100-million years of "domestication," the virus has become completely integrated within the wasp's physiology.

To date, this total physiological integration of complex viruses has only been demonstrated in parasitic wasps. Nonetheless, the mechanism may be much more widespread in nature, conferring an array of organisms with novel functions such as gene or protein delivery via viral particles or envelopes.

The parasitic nature of Cotesia wasps is currently harnessed in agriculture to control crop damage done by lepidopteran larvae. For example, since the 1980s, these wasps are used extensively in Brazil to protect millions of hectares of sugar cane against sugarcane borers, a pest species that is difficult to control with pesticides. The study done by this international consortium brings new fundamental knowledge on the genetic and evolutionary nature of this agriculturally beneficial family of wasps, and will thus contribute to the development and advancement of sustainable crop production.

1 – French members of the consortium:  l’Institut de recherche sur la biologie de l'insecte (IRBI – CNRS / Université de Tours), le laboratoire Génétique des génomes (CNRS / Institut Pasteur), l’Institut d'écologie et des sciences de l'environnement de Paris (iEES – CNRS / Sorbonne Université / Univ. Paris-Est Créteil Val-de-Marne / INRAE / IRD), le Genoscope (CEA / Université Paris-Saclay / Université Evry-Val-d’Essonne), le laboratoire de biométrie et biologie évolutive (LBBE – CNRS / Université Claude Bernard / Vetagro Sup), et le laboratoire Évolution, génomes, comportement et écologie (EGCE – CNRS / IRD / Université Paris-Saclay)
2 - Genoscope / Institut de Biologie François Jacob du CEA (CEA / Université Paris-Saclay / Université Evry-Val-d’Essonne)

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