Allelic Variation in a Single Genomic Region Alters the Microbiome of the Snail Biomphalaria glabrata

Abstract

Freshwater snails are the intermediate hosts for numerous parasitic worms which can have negative consequences for human health and agriculture. Understanding the transmission of these diseases requires a more complete characterization of the immunobiology of snail hosts. This includes the characterization of its microbiome and genetic factors which may interact with this important commensal community. Allelic variation in the Guadeloupe resistance complex (GRC) genomic region of Guadeloupean Biomphalaria glabrata influences their susceptibility to schistosome infection and may have other roles in the snail immune response. In the present study, we examined whether a snail's GRC genotype has a role in shaping the bacterial diversity and composition present on or in whole snails. We show that the GRC haplotype, including the resistant genotype, has a significant effect on the diversity of bacterial species present in or on whole snails, including the relative abundances of Gemmatimonas aurantiaca and Micavibrio aeruginosavorus. These findings support the hypothesis that the GRC region is likely involved in pathways that can modify the microbial community of these snails and may have more immune roles in B. glabrata than originally believed. This is also one of few examples in which allelic variation at a particular locus has been shown to affect the microbiome in any species.

Figure 1.

Allelic variation in the GRC region influences the microbiome of BgGUA. (A) OTU composition of the microbiome in homozygous inbred lines (isolated from each other for >3 years; n = 12 RR, 7 S1S1, and 11 S2S2 lines) of BgGUA, as depicted with NMDS of OTUs generated. Overall community composition of S1S1 is significantly different (PERMANOVA Bray–Curtis, P = 0.03) from the other 2 genotypes, although all 3 genotypes show similarly high variability and did not have differing diversity (H). The relative abundance of Micavibrio aeruginosavorus ARL-13 is significantly different in RR lines (uncorrected P = 1.8e-04; α = 0.05/223 = 2.2e-04). (B) OTU composition of the microbiome in outbred BgGUA (2 tanks separated for >1 year) (tank 1: n = 5 S2S2, 7 S1S2, 4 S1R, 14 RR, 19 S2R; tank 2: n = 15 S2S2, 3 S1S2, 6 S1R, 10 RR, 12 S2R), as depicted with NMDS. Allelic variation in the GRC region has no significant influence on the OTU composition or abundance but a significant difference in diversity (H, P = 0.04). All genotypes show similarly high variability.

Figure 2.

Allelic variation in the GRC region influences the relative abundance of Micavibrio aeruginosavorus and Gemmatimonas aurantiaca. P-values for the top 29 OTUs in inbred and outbred experiments (Wilcoxon rank-sum test). All OTUs with P <0.05 in either experiment are shown, plotted on a negative log scale for each experiment. The dotted lines represent P = 0.05. The solid line shows where combined P-values are significant at a Bonferroni corrected α of 2.2e-04. Two OTUs show a significant combined P-value (Fisher’s combined P): M. aeruginosavorus ARL-13 (P = 2.4e-05) and G. aurantiaca T-27 (P = 9.9e-05).