Abstract
The co-evolutionary dynamics that exist in certain invertebrate host / parasite interactions sometimes lead to a compatibility polymorphism, of which the molecular bases are unknown. To identify key molecules involved in this phenomenon in the Schistosoma mansoni / Biomphalaria glabrata model, we developed a comparative proteomics approach for the larval stages that interact with the invertebrate host. The qualitative and quantitative comparison of the proteomes of compatible and incompatible parasite strains led to the identification of a new family of schistosome antigens that share molecular characteristics with highly glycosylated secreted mucins. In particular, they possess a domain containing a variable number of tandem repeats (VNTR). These proteins are (i) only expressed in larval stages interacting with the mollusc, (ii) located in the apical gland of miracidia and sporocysts and (iii) secreted and released in excretion-secretion products. Moreover, we show that these mucin-like proteins display a high degree of polymorphism and that extensive differences are observed between S. mansoni strains. These different characteristics led us to name this novel molecular family "S. mansoni Polymorphic Mucins" SmPoMuc. Next, we show that SmPoMuc are coded by a multi-gene family that evolve following the model of "birth and death". SmPoMuc genes are transcribed in an individual-specific manner, and for each gene, multiple splice variants exist. The incidence of this polymorphism on SmPoMuc glycosylation status was demonstrated. Our data support the view that S. mansoni has evolved a complex cascade of mechanisms - a "controlled chaos" - based on a relatively low number of genes that provides highly polymorphism to SmPoMuc