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

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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. Contrary to the traditional view that immunity in invertebrates is limited to non-specific mechanisms, recent studies have shown that they have diverse, specific immune receptors. An example is provided by the FREPs of the mollusk Biomphalaria glabrata, polymorphic members of the immunoglobulin superfamily. This capacity for an individual or population-based polymorphic immune response raises the question of whether a corresponding polymorphism exists in parasites of invertebrates, as would be expected in an “arms race” between host and parasite. We have indeed identified such polymorphic molecules in Schistosoma mansoni, a flatworm parasite of B. glabrata, by comparing two strains of schistosome that are respectively compatible and incompatible with the same mollusk host strain. However, in contrast to antigenic variation in protozoan parasites that is based on an extensive gene repertoire, we show here that a high level of polymorphism in these S. mansoni polymorphic mucins (SmPoMucs) is generated from a low number of genes by a complex cascade of mechanisms, a “controlled chaos”.

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