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

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.

An example of molecular co-evolution: Reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions

“…At present, however, there is relatively little empirical evidence demonstrating reciprocal molecular adaptations in both host and parasite. Here, we investigated the interaction between S. mansoni and the snail, B. glabrata, as this interaction is a popular model for the study of co-evolutionary dynamics Bouchut et al, 2008;Roger et al, 2008a;Roger et al, 2008b;Roger et al, 2008c;Steinauer, 2009). We confirmed that there are different levels of compatibility between two geographic strains of S. mansoni and their sympatric snail hosts, B. glabrata (Fig.…”

Use of OmpU porins for attachment and invasion of Crassostrea gigas immune cells by the oyster pathogen Vibrio splendidus

“…As such, they are equipped with immune receptors and effectors involved in pathogen recognition and control. Recent advances in molluskpathogen interactions have shown the existence of highly diverse somatically generated receptors that give high specificity to pathogen recognition (16,17). So far, in oysters, recognition is mediated by germ-line encoded receptors, such as a β-integrin, involved in hemocyte phagocytosis (18); it was proposed to serve as a receptor for the major plasma protein, the extracellular superoxide dismutase Cg-EcSOD, which contains a RGD cellbinding domain (19).…”

Towards an understanding of the epigenetics of schistosomes: a comparative epigenomic study

“…Its potential role in the context of immune evasion strategy has been previously discussed (DeMarco et al 2010). It is of particular interest that MEG-2 shares many common features with the SmPoMuc genes, previously described as major molecular determinants for the compatibility polymorphism (Roger et al 2008b). SmPoMuc genes encode highly polymorphic glycosylated proteins that are secreted in miracidia and their cDNA variants seem to be generated by the "pick and mix" strategy as described for the MEG genes (Berriman et al 2009).…”