Combining a transcriptomic approach and a targeted metabolomics approach for deciphering the molecular bases of compatibility phenotype in the snail Biomphalaria glabrata toward Schistosoma mansoni.

Biomphalaria glabrata is a freshwater snail and the obligatory intermediate host of Schistosoma mansoni parasite, the etiologic agent of intestinal Schistosomiasis, in South America and Caribbean. Interestingly in such host-parasite interactions, compatibility varies between populations, strains or individuals. This observed compatibility polymorphism is based on a complex molecular-matching-phenotype, the molecular bases of which have been investigated in numerous studies, notably by comparing between different strains or geographical isolates or clonal selected snail lines. Herein we propose to decipher the constitutive molecular support of this interaction in selected non-clonal resistant and susceptible snail strain originating from the same natural population from Brazil and thus having the same genetic background. Thanks to a global RNAseq transcriptomic approach on whole snail, we identified a total of 328 differentially expressed genes between resistant and susceptible phenotypes among which 129 were up-regulated and 199 down-regulated. Metabolomic studies were used to corroborate the RNAseq results. The activation of immune genes and specific metabolic pathways in resistant snails might provide them with the capacity to better respond to parasite infection.

Hyperdiverse gene cluster in snail host conveys resistance to human schistosome parasites.

Schistosomiasis, a neglected global pandemic, may be curtailed by blocking transmission of the parasite via its intermediate hosts, aquatic snails. Elucidating the genetic basis of snail-schistosome interaction is a key to this strategy. Here we map a natural parasite-resistance polymorphism from a Caribbean population of the snail Biomphalaria glabrata. In independent experimental evolution lines, RAD genotyping shows that the same genomic region responds to selection for resistance to the parasite Schistosoma mansoni. A dominant allele in this region conveys an 8-fold decrease in the odds of infection. Fine-mapping and RNA-Seq characterization reveal a <1Mb region, the Guadeloupe Resistance Complex (GRC), with 15 coding genes. Seven genes are single-pass transmembrane proteins with putative immunological roles, most of which show strikingly high nonsynonymous divergence (5-10%) among alleles. High linkage disequilibrium among three intermediate-frequency (>25%) haplotypes across the GRC, a significantly non-neutral pattern, suggests that balancing selection maintains diversity at the GRC. Thus, the GRC resembles immune gene complexes seen in other taxa and is likely involved in parasite recognition. The GRC is a potential target for controlling transmission of schistosomiasis, including via genetic manipulation of snails.