Research Article: Controlled Chaos of Polymorphic Mucins in a Metazoan Parasite (Schistosoma mansoni) Interacting with Its Invertebrate Host (Biomphalaria glabrata)

Date Published: November 11, 2008

Publisher: Public Library of Science

Author(s): Emmanuel Roger, Christoph Grunau, Raymond J. Pierce, Hirohisa Hirai, Benjamin Gourbal, Richard Galinier, Rémi Emans, Italo M. Cesari, Céline Cosseau, Guillaume Mitta, Paul J. Brindley

Abstract: Invertebrates were long thought to possess only a simple, effective and hence non-adaptive defence system against microbial and parasitic attacks. However, recent studies have shown that invertebrate immunity also relies on immune receptors that diversify (e.g. in echinoderms, insects and mollusks (Biomphalaria glabrata)). Apparently, individual or population-based polymorphism-generating mechanisms exists that permit the survival of invertebrate species exposed to parasites. Consequently, the generally accepted arms race hypothesis predicts that molecular diversity and polymorphism also exist in parasites of invertebrates. We investigated the diversity and polymorphism of parasite molecules (Schistosoma mansoni Polymorphic Mucins, SmPoMucs) that are key factors for the compatibility of schistosomes interacting with their host, the mollusc Biomphalaria glabrata. We have elucidated the complex cascade of mechanisms acting both at the genomic level and during expression that confer polymorphism to SmPoMuc. We show that SmPoMuc is coded by a multi-gene family whose members frequently recombine. We show that these genes are transcribed in an individual-specific manner, and that for each gene, multiple splice variants exist. Finally, we reveal the impact of this polymorphism on the SmPoMuc glycosylation status. Our data support the view that S. mansoni has evolved a complex hierarchical system that efficiently generates a high degree of polymorphism—a “controlled chaos”—based on a relatively low number of genes. This contrasts with protozoan parasites that generate antigenic variation from large sets of genes such as Trypanosoma cruzi, Trypanosoma brucei and Plasmodium falciparum. Our data support the view that the interaction between parasites and their invertebrate hosts are far more complex than previously thought. While most studies in this matter have focused on invertebrate host diversification, we clearly show that diversifying mechanisms also exist on the parasite side of the interaction. Our findings shed new light on how and why invertebrate immunity develops.

Partial Text: The comprehension of host-parasite interactions represents a major challenge in evolutionary biology. Parasites are responsible for substantial deleterious effects on their hosts, and therefore represent a major driving force for their evolution. In parallel, parasites have to cope with the evolving host-defence mechanisms, i.e. they must co-evolve with their host to avoid elimination. This adaptation of the Red Queen hypothesis [1] to host-parasite systems predicts that an arms race takes place in which both host and parasite develop mechanisms that generate diversity and polymorphism of molecules that play key roles in the host-parasite interplay [2].

SmPoMucs are mucin-like molecules that we recently discovered by a proteomics approach aiming at identifying molecular determinants of compatibility polymorphism in the interaction between S. mansoni and its intermediate host B. glabrata[17]. The comparison of the proteomes of sporocysts (intramolluskan stage) of two S. mansoni strains, one compatible with a specific strain of B. glabrata, the other incompatible with the same mollusk strain, showed that the principal difference lies in this protein family with the characteristics of mucins. We showed that these proteins are glycosylated, expressed in the apical gland of S. mansoni miracidia and sporocysts and are present in their Excretion-Secretion products [18]. These molecules are highly polymorphic and we therefore called them SmPoMucs for S. mansoni polymorphic mucins. In the present study, we have extended the analysis of their polymorphism and show that each individual larva expresses a unique combination of SmPoMucs derived from a limited set of genes. This extraordinary level of polymorphism may be linked to (i) gene structure, organization and evolution, and/or (ii) different regulation processes occurring during gene expression. In this study we have elucidated the complex cascade of mechanisms that confer polymorphism to SmPoMuc.



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