A genome sequence for Biomphalaria pfeifferi, the major vector snail for the human-infecting parasite Schistosoma mansoni

Abstract

Background

Biomphalaria pfeifferi is the world’s most widely distributed and commonly implicated vector snail species for the causative agent of human intestinal schistosomiasis, Schistosoma mansoni. In efforts to control S. mansoni transmission, chemotherapy alone has proven insufficient. New approaches to snail control offer a way forward, and possible genetic manipulations of snail vectors will require new tools. Towards this end, we here offer a diverse set of genomic resources for the important African schistosome vector, B. pfeifferi.

Methodology/Principal findings

Based largely on PacBio High-Fidelity long reads, we report a genome assembly size of 772 Mb for B. pfeifferi (Kenya), smaller in size than known genomes of other planorbid schistosome vectors. In a total of 505 scaffolds (N50 = 3.2Mb), 430 were assigned to 18 large linkage groups inferred to represent the 18 known chromosomes, based on whole genome comparisons with Biomphalaria glabrata. The annotated B. pfeifferi genome reveals a divergence time of 3.01 million years with B. glabrata, a South American species believed to be similar to the progenitors of B. pfeifferi which undertook a trans-Atlantic colonization < five million years ago.

Conclusions/Significance

The genome for this preferentially self-crossing species is less heterozygous than related species known to be preferential out-crossers; its smaller genome relative to congeners may similarly reflect its preference for selfing. Expansions of gene families with immune relevance are noted, including the FReD gene family which is far more similar in its composition to B. glabrata than to Bulinus truncatus, a vector for Schistosoma haematobium. Provision of this annotated genome will help better understand the dependencies of trematodes on snails, enable broader comparative insights regarding factors contributing to susceptibility/ resistance of snails to schistosome infections, and provide an invaluable resource with respect to identifying and manipulating snail genes as potential targets for more specific snail control programs.

Author summary

Biomphalaria pfeifferi is the world’s most widely distributed and commonly implicated vector snail for the causative agent of human intestinal schistosomiasis, Schistosoma mansoni. Understanding the basis of host-parasite compatibility relies on functional genomic resources, which will be helpful for developing genetic-based control of schistosomes and their vector snails. Here we report a high-quality, de novo–assembled whole genome for B. pfeifferi (PacBio High-Fidelity long reads), with in-depth gene model annotation for protein-coding and nonprotein-coding genes. Using these enriched molecular data, a divergence date of 3.01 Mya was calculated for B. pfeifferi and B. glabrata, consistent with the idea of Biomphalaria colonization of Africa from South America, and placing an upper boundary on the age of S. mansoni in Africa. The spread of S. mansoni was likely favored by its high degree of compatibility with B. pfeifferi-like snails. In addition, our evidence supports the idea that B. pfeifferi is a preferentially self-crossing species with a more homozygous and smaller genome than related species like B. glabrata known to be preferential out-crossers. Furthermore, several immune-related gene families have expanded differently between B. pfeifferi to B. glabrata. Resources provided here will deepen our general knowledge of molluscan biology, host-parasite co-evolution, vector biology, and genomics.