Multi-strain compatibility polymorphism between a parasite and its snail host, a neglected vector of schistosomiasis in Africa

Spaan, Johannie M.; Pennance, Tom; Laidemitt, Martina R.; Sims, Nicole; Roth, Jewell; Lam, Yvonne Y. H.; Rawago, Fredrick; Ogara, George; Loker, Eric S.; Odiere, Maurice R.; Steinauer, Michelle L.

doi:10.1016/j.crpvbd.2023.100120

Cited by 2 publications

(2 citation statements)

References 51 publications

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“…The line Bs163 was the most divergent, with an average genomic divergence value of 0.44% from the four other inbred lines (Bs111, Bs110, BsKEMRI and Bs5-2). The Bs163 line is also the most resistant to S. mansoni infection in the laboratory [ 78 ]. Among the remaining four, pairwise divergences were similar and ranged between 0.28% and 0.41% with one exception: Bs110 and Bs111 were only 0.16% divergent showing high similarity.…”

Section: Resultsmentioning

confidence: 99%

The genome and transcriptome of the snail Biomphalaria sudanica s.l.: immune gene diversification and highly polymorphic genomic regions in an important African vector of Schistosoma mansoni

Pennance,

Calvelo,

Tennessen

et al. 2024

BMC Genomics

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Background Control and elimination of schistosomiasis is an arduous task, with current strategies proving inadequate to break transmission. Exploration of genetic approaches to interrupt Schistosoma mansoni transmission, 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 genus Biomphalaria. Few complete genomic resources exist, with African Biomphalaria species being particularly underrepresented despite this being where the majority of S. mansoni infections occur. Here we generate and annotate the first genome assembly of Biomphalaria sudanica sensu lato, a species responsible for S. mansoni transmission 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 vector B. glabrata and present a bioinformatic pipeline to identify candidate novel pathogen recognition receptors (PRRs). Results De novo genome and transcriptome assembly of inbred B. sudanica originating from the shoreline of Lake Victoria (Kisumu, Kenya) resulted in a haploid genome size of ~ 944.2 Mb (6,728 fragments, N50 = 1.067 Mb), comprising 23,598 genes (BUSCO = 93.6% complete). The B. sudanica genome contains orthologues to all described immune genes/regions tied to protection against S. mansoni in B. glabrata, including the polymorphic transmembrane clusters (PTC1 and PTC2), RADres, and other loci. The B. sudanica PTC2 candidate immune genomic region contained many PRR-like genes across a much wider genomic region than has been shown in B. glabrata, as well as a large inversion between species. High levels of intra-species nucleotide diversity were seen in PTC2, as well as in regions linked to PTC1 and RADres orthologues. Immune related and putative PRR gene families were significantly over-represented in the sub-set of B. sudanica genes 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 was seen in African compared to South American lineages. Conclusions The B. sudanica genome 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.

show abstract

Section: Resultsmentioning

confidence: 99%

The genome and transcriptome of the snail Biomphalaria sudanica s.l.: immune gene diversification and highly polymorphic genomic regions in an important African vector of Schistosoma mansoni

Pennance,

Calvelo,

Tennessen

et al. 2024

BMC Genomics

Self Cite

View full text Add to dashboard Cite

show abstract

“…The line Bs163 was the most divergent, with an average genomic divergence value of 0.44% from the four other inbred lines (Bs111, Bs110, BsKEMRI and Bs5-2). The Bs163 line is also the most resistant to S. mansoni infection in the laboratory setting (77). Among the remaining four, pairwise divergences were similar and ranged between 0.28% and 0.41% with one exception: Bs110 and Bs111 were only 0.16% divergent showing high similarity.…”

Section: Intraspecific Diversity Of the B Sudanica Genome: Comparing ...mentioning

confidence: 97%

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

Pennance,

Calvelo,

Tennessen

et al. 2023

Preprint

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BackgroundControl 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.

show abstract

Multi-strain compatibility polymorphism between a parasite and its snail host, a neglected vector of schistosomiasis in Africa

Cited by 2 publications

References 51 publications

The genome and transcriptome of the snail Biomphalaria sudanica s.l.: immune gene diversification and highly polymorphic genomic regions in an important African vector of Schistosoma mansoni

The genome and transcriptome of the snail Biomphalaria sudanica s.l.: immune gene diversification and highly polymorphic genomic regions in an important African vector of Schistosoma mansoni

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

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