Allelic variation in a single genomic region alters the hemolymph proteome in the snail Biomphalaria glabrata

Abstract

Freshwater snails are obligate intermediate hosts for numerous parasitic trematodes, most notably schistosomes. Schistosomiasis is a devastating human and veterinary illness, which is primarily controlled by limiting the transmission of these parasites from their intermediate snail hosts. Understanding how this transmission occurs, as well as the basic immunobiology of these snails may be important for controlling this disease in the future. Allelic variation in the Guadeloupe resistance complex (GRC) of Biomphalaria glabrata partially determines their susceptibility to parasitic infection, and can influence the microbiome diversity and microbial defenses in the hemolymph of these snails. In the present study, we examine the most abundant proteins present in the hemolymph of snails that are resistant or susceptible to schistosomes, as determined by their GRC genotype. Using proteomic analysis, we found that snails with different GRC genotypes have differentially abundant hemolymph proteins that are not explained by differences in transcription. There are 13 revealed hemolymph proteins that differ significantly between resistant and susceptible genotypes, nearly 40% of which are involved in immune responses. These findings build on the mounting evidence that genes in the GRC region have multiple physiological roles, and likely contribute more extensively to the general immune response than previously believed. These data also raise the intriguing possibility that the GRC region controls resistance to schistosomes, not directly, but indirectly via its effects on the snail's proteome and potentially its microbiome.

Keywords: Allelic variation; Biomphalaria glabrata; Hemolymph; Proteomics.

Fig 1.. The hemolymph proteome clusters by GRC genotype in BgGUA.

A 2D scores plot of the principal component analysis (PCA) for the proteomic profile of pooled hemolymph. Each point represents pooled hemolymph from 20 snails from each of 15 independent inbred lines: RR, S1S1, S2S2 (n =5 lines/genotype).

Fig 2.. Expression of the genes coding for the 13 proteins revealed by proteomic analysis to differ significantly between RR and SS genotypes.

The relative expression of mRNA for 13 genes corresponding to 13 revealed hemolymph proteins from outbred RR (n = 18), S1S1 (n = 9), S2S2 (n = 9). Each sample point represents expression data from an individual snail sampled from our outbred population. Per-sample/site depth expression is shown for all three genotypes (log-scale). No significant differences were observed (ANOVA, Bonferroni adjusted p>0.003).