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Open Access Research article

Viral cystatin evolution and three-dimensional structure modelling: A case of directional selection acting on a viral protein involved in a host-parasitoid interaction

Céline Serbielle1, Shafinaz Chowdhury2, Samuel Pichon14, Stéphane Dupas3, Jérôme Lesobre14, Enrico O Purisima2, Jean-Michel Drezen1 and Elisabeth Huguet1*

Author Affiliations

1 Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 6035, Faculté des Sciences et Techniques, Parc de Grandmont, 37200 Tours, France

2 National Research Council Canada, Biotechnology Research Institute, Montreal, Canada

3 Institut de Recherche pour le Développement, Quito, Ecuador

4 Laboratoire Ecologie Evolution Symbiose, UMR 6556, Université de Poitiers, Poitiers, France

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BMC Biology 2008, 6:38  doi:10.1186/1741-7007-6-38

Published: 10 September 2008

Abstract

Background

In pathogens, certain genes encoding proteins that directly interact with host defences coevolve with their host and are subject to positive selection. In the lepidopteran host-wasp parasitoid system, one of the most original strategies developed by the wasps to defeat host defences is the injection of a symbiotic polydnavirus at the same time as the wasp eggs. The virus is essential for wasp parasitism success since viral gene expression alters the immune system and development of the host. As a wasp mutualist symbiont, the virus is expected to exhibit a reduction in genome complexity and evolve under wasp phyletic constraints. However, as a lepidopteran host pathogenic symbiont, the virus is likely undergoing strong selective pressures for the acquisition of new functions by gene acquisition or duplication. To understand the constraints imposed by this particular system on virus evolution, we studied a polydnavirus gene family encoding cyteine protease inhibitors of the cystatin superfamily.

Results

We show that cystatins are the first bracovirus genes proven to be subject to strong positive selection within a host-parasitoid system. A generated three-dimensional model of Cotesia congregata bracovirus cystatin 1 provides a powerful framework to position positively selected residues and reveal that they are concentrated in the vicinity of actives sites which interact with cysteine proteases directly. In addition, phylogenetic analyses reveal two different cystatin forms which evolved under different selective constraints and are characterized by independent adaptive duplication events.

Conclusion

Positive selection acts to maintain cystatin gene duplications and induces directional divergence presumably to ensure the presence of efficient and adapted cystatin forms. Directional selection has acted on key cystatin active sites, suggesting that cystatins coevolve with their host target. We can strongly suggest that cystatins constitute major virulence factors, as was already proposed in previous functional studies.