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
Abstract 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-Sahara...
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| Format: | Article |
| Language: | English |
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BMC
2024-02-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-024-10103-w |
| _version_ | 1827328486479495168 |
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| author | Tom Pennance Javier Calvelo Jacob A. Tennessen Ryan Burd Jared Cayton Stephanie R. Bollmann Michael S. Blouin Johannie M. Spaan Federico G. Hoffmann George Ogara Fredrick Rawago Kennedy Andiego Boaz Mulonga Meredith Odhiambo Eric S. Loker Martina R. Laidemitt Lijun Lu Andrés Iriarte Maurice R. Odiere Michelle L. Steinauer |
| author_facet | Tom Pennance Javier Calvelo Jacob A. Tennessen Ryan Burd Jared Cayton Stephanie R. Bollmann Michael S. Blouin Johannie M. Spaan Federico G. Hoffmann George Ogara Fredrick Rawago Kennedy Andiego Boaz Mulonga Meredith Odhiambo Eric S. Loker Martina R. Laidemitt Lijun Lu Andrés Iriarte Maurice R. Odiere Michelle L. Steinauer |
| author_sort | Tom Pennance |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-03-07T15:18:36Z |
| format | Article |
| id | doaj.art-060b7a186267402a98b79932cf522cff |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-07T15:18:36Z |
| publishDate | 2024-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-060b7a186267402a98b79932cf522cff2024-03-05T17:46:33ZengBMCBMC Genomics1471-21642024-02-0125112810.1186/s12864-024-10103-wThe 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 mansoniTom Pennance0Javier Calvelo1Jacob A. Tennessen2Ryan Burd3Jared Cayton4Stephanie R. Bollmann5Michael S. Blouin6Johannie M. Spaan7Federico G. Hoffmann8George Ogara9Fredrick Rawago10Kennedy Andiego11Boaz Mulonga12Meredith Odhiambo13Eric S. Loker14Martina R. Laidemitt15Lijun Lu16Andrés Iriarte17Maurice R. Odiere18Michelle L. Steinauer19College of Osteopathic Medicine of the Pacific – Northwest, Western University of Health SciencesLaboratorio de Biología Computacional, Departamento de Desarrollo Biotecnológico, Facultad de Medicina, Instituto de Higiene, Universidad de La RepúblicaHarvard T.H. Chan School of Public HealthCollege of Osteopathic Medicine of the Pacific – Northwest, Western University of Health SciencesCollege of Osteopathic Medicine of the Pacific – Northwest, Western University of Health SciencesOregon State UniversityOregon State UniversityCollege of Osteopathic Medicine of the Pacific – Northwest, Western University of Health SciencesDepartment of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State UniversityCentre for Global Health Research, Kenya Medical Research Institute (KEMRI)Centre for Global Health Research, Kenya Medical Research Institute (KEMRI)Centre for Global Health Research, Kenya Medical Research Institute (KEMRI)Centre for Global Health Research, Kenya Medical Research Institute (KEMRI)Centre for Global Health Research, Kenya Medical Research Institute (KEMRI)Center for Evolutionary and Theoretical Immunology, Parasite Division Museum of Southwestern Biology, Department of Biology, University of New MexicoCenter for Evolutionary and Theoretical Immunology, Parasite Division Museum of Southwestern Biology, Department of Biology, University of New MexicoCenter for Evolutionary and Theoretical Immunology, Parasite Division Museum of Southwestern Biology, Department of Biology, University of New MexicoLaboratorio de Biología Computacional, Departamento de Desarrollo Biotecnológico, Facultad de Medicina, Instituto de Higiene, Universidad de La RepúblicaCentre for Global Health Research, Kenya Medical Research Institute (KEMRI)College of Osteopathic Medicine of the Pacific – Northwest, Western University of Health SciencesAbstract 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.https://doi.org/10.1186/s12864-024-10103-wBiomphalaria sudanicaBiomphalaria choanomphalaSchistosomiasisSnail vectorDe novo genome assemblyPolymorphism |
| spellingShingle | Tom Pennance Javier Calvelo Jacob A. Tennessen Ryan Burd Jared Cayton Stephanie R. Bollmann Michael S. Blouin Johannie M. Spaan Federico G. Hoffmann George Ogara Fredrick Rawago Kennedy Andiego Boaz Mulonga Meredith Odhiambo Eric S. Loker Martina R. Laidemitt Lijun Lu Andrés Iriarte Maurice R. Odiere Michelle L. Steinauer 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 BMC Genomics Biomphalaria sudanica Biomphalaria choanomphala Schistosomiasis Snail vector De novo genome assembly Polymorphism |
| title | 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 |
| title_full | 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 |
| title_fullStr | 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 |
| title_full_unstemmed | 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 |
| title_short | 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 |
| title_sort | 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 |
| topic | Biomphalaria sudanica Biomphalaria choanomphala Schistosomiasis Snail vector De novo genome assembly Polymorphism |
| url | https://doi.org/10.1186/s12864-024-10103-w |
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