Dietary variations drive divergent phenotypic, transcriptomic, and metatranscriptomic profiles in Biomphalaria glabrata, a schistosomiasis vector snail.

Abstract

The freshwater snail Biomphalaria glabrata is an important natural vector for the human parasitic trematode Schistosoma mansoni, which causes schistosomiasis. In the laboratory, B. glabrata are routinely maintained on simple lettuce diets. We aimed to explore and compare the impact of alternative diets on snail performance, global gene expression, and microbiome. Snails were raised in groups on fresh lettuce (FL), fish food (FF), and artificial snail gel (SG) diets for 8 weeks, while measuring dietary impacts on growth, survival, and fecundity. RNA sequencing (RNA-Seq) was performed to correlate dietary phenotypes with changes in the snail transcriptome and associated microbial metatranscriptome. Fish food (FF) and SG diets markedly enhanced snail growth, survival, and fecundity, with FF generating the highest fecundity rate. RNA-Seq identified 21,887 expressed genes in the snail's transcriptome. Of these, diet significantly modulated 6501 genes (padj < 0.01), representing 13.0% of the predicted genes in the B. glabrata genome. Fish food (FF) and SG diets drove upregulation of genes associated with antimicrobial immunity, growth, and reproduction, while elevated expression of genes linked to xenobiotic metabolism and oxidative stress was observed in FL-fed snails. Metatranscriptomic analysis identified 104 microbial classes, with a total of 23 classes significantly enriched in FF and SG snails, including short-chain fatty acid (SCFA)-producing and nutrient-cycling bacteria. A significant correlation (r = 0.63, P = 0.001) linked differentially expressed genes to enriched microbial transcripts, highlighting the impact of diet on key snail health and performance metrics. This work is the first nutritranscriptomic analysis of laboratory-bred B. glabrata. We describe key insights into the diet-phenotype-transcriptome-microbiome axis, which will inform dietary precision and optimisation for laboratory culture of B. glabrata. These data also highlight fundamental aspects of snail biology that could be exploited for molecular snail control approaches.