The genome and transcriptome of the snailBiomphalaria sudanica s.l.: Immune gene diversification and highly polymorphic genomic regions in an important African vector ofSchistosoma mansoni

Abstract

AbstractBackgroundControl and elimination of schistosomiasis is an arduous task, with current strategies proving inadequate to break transmission. Exploration of genetic approaches to interruptSchistosoma mansonitransmission, the causative agent for human intestinal schistosomiasis in sub-Saharan Africa and South America, has led to genomic research of the snail vector hosts of the genusBiomphalaria. Few complete genomic resources exist, with AfricanBiomphalariaspecies being particularly underrepresented despite this being where the majority ofS. mansoniinfections occur. Here we generate and annotate the first genome assembly ofBiomphalaria sudanicasensu lato, a species responsible forS. mansonitransmission in lake and marsh habitats of the African Rift Valley. Supported by whole-genome diversity data among five inbred lines, we describe orthologs of immune-relevant gene regions in the South American vectorB. glabrataand present a bioinformatic pipeline to identify candidate novel pathogen recognition receptors (PRRs).ResultsDe novogenome and transcriptome assembly of inbredB. sudanicaoriginating from the shoreline of Lake Victoria (Kisumu, Kenya) resulted in a haploid genome size of ∼944.2 Mb (6732 fragments, N50=1.067 Mb), comprising 23,598 genes (BUSCO=93.6% complete). TheB. sudanicagenome contains orthologues to all described immune genes/regions tied to protection againstS. mansoniinB. glabrata. TheB. sudanica PTC2candidate immune genomic region contained many PRR-like genes across a much wider genomic region than has been shown inB. glabrata, as well as a large inversion between species. High levels of intra-species nucleotide diversity were seen inPTC2, as well as in regions linked toPTC1andRADresorthologues. Immune related and putative PRR gene families were significantly over-represented in the sub-set ofB. sudanicagenes determined as hyperdiverse, including high extracellular diversity in transmembrane genes, which could be under pathogen-mediated balancing selection. However, no overall expansion in immunity related genes were seen in African compared to South American lineages.ConclusionsTheB. sudanicagenome and analyses presented here will facilitate future research in vector immune defense mechanisms against pathogens. This genomic/transcriptomic resource provides necessary data for the future development of molecular snail vector control/surveillance tools, facilitating schistosome transmission interruption mechanisms in Africa.