{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T01:16:03Z","timestamp":1760058963091,"version":"build-2065373602"},"reference-count":92,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T00:00:00Z","timestamp":1747353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, the Shanghai Municipal Education Commission","award":["2021YFC2300800","2021YFC2300804"],"award-info":[{"award-number":["2021YFC2300800","2021YFC2300804"]}]},{"name":"National Key Research and Development Program of the Republic of China","award":["2021YFC2300800","2021YFC2300804"],"award-info":[{"award-number":["2021YFC2300800","2021YFC2300804"]}]},{"name":"Scientific Research and Innovation Directorate, Ministry of Higher Education and Scientific Research, Sudan","award":["2021YFC2300800","2021YFC2300804"],"award-info":[{"award-number":["2021YFC2300800","2021YFC2300804"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Biomphalaria pfeifferi is a key intermediate host for Schistosoma\u00a0mansoni transmission in Sudan. In total, 27 complete mitochondrial genomes from seven B. pfeifferi populations in Gezira State, Sudan, were sequenced for the first time to investigate their population structure and phylogenetic relationships. This involved comparing the nucleotide composition, codon usage, rRNAs, and tRNAs of the East Gezira (EG), South Gezira (SG), Hasahisa (HA), Greater Wad Medani (GW), Managil (MA), and North Umelgura (NU1, NU3) populations. All 27 mitogenomes (13,688\u201313,696 bp) contained 37 genes with conserved AT\/GC content (76.7\/23.4%). Phylogenetic analysis revealed that although samples clustered within the same clade, B. pfeifferi from EG, SG, NU1, and NU3 grouped closely with B. pfeifferi from Kenya, whereas HA and GW samples formed distinct ancestral lineages. The MA population exhibited unique genetic characteristics, supported by phylogenetic trees and nucleotide\/amino acid identity, suggesting the potential presence of a distinct B. pfeifferi subspecies that warrants further investigation. All protein-coding genes evolved under negative selection, with the amino acids of nad1 and nad6 being highly conserved, while nad3 exhibited some variation. Further research on the mitogenomic diversity of B. pfeifferi and other Biomphalaria species in Sudan and across Africa is needed in order to better understand the population structure and evolutionary history of Biomphalaria.<\/jats:p>","DOI":"10.3390\/ijms26104756","type":"journal-article","created":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T05:11:57Z","timestamp":1747372317000},"page":"4756","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Comparative Mitochondrial Genome Analysis of the Intestinal Schistosomiasis Snail Host Biomphalaria pfeifferi from Multiple Populations in Gezira State, Sudan"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0009-0006-4518-0510","authenticated-orcid":false,"given":"Arwa","family":"Osman","sequence":"first","affiliation":[{"name":"State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China"},{"name":"Blue Nile National Institute for Communicable Diseases, University of Gezira, P.O. Box 20, Wad Madani 5118 40466, Sudan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9922-7891","authenticated-orcid":false,"given":"Peter S.","family":"Andrus","sequence":"additional","affiliation":[{"name":"National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai 200025, China"},{"name":"School of Global Health, Chinese Centre for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6941-1471","authenticated-orcid":false,"given":"Xianglu","family":"Zhu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhaoyang","family":"Dong","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yunhai","family":"Guo","sequence":"additional","affiliation":[{"name":"National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai 200025, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bakri Y. M.","family":"Nour","sequence":"additional","affiliation":[{"name":"Faculty of Medical Laboratories, University of Gezira, P.O. Box 20, Wad Madani 5118 40466, Sudan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaonong","family":"Zhou","sequence":"additional","affiliation":[{"name":"National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai 200025, China"},{"name":"School of Global Health, Chinese Centre for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8523-103X","authenticated-orcid":false,"given":"Liming","family":"Zhao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Brown, D.S. (1994). Freshwater Snails of Africa and Their Medical Importance, CRC Press.","DOI":"10.1201\/9781482295184"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3041","DOI":"10.1046\/j.1365-294X.2003.01977.x","article-title":"Phylogeography of Biomphalaria glabrata and B. pfeifferi, Important Intermediate Hosts of Schistosoma mansoni in the New and Old World Tropics","volume":"12","author":"Dejong","year":"2003","journal-title":"Mol. Ecol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Au, M.F.F. (2023). Status Quo and Future Perspectives of Molecular and Genomic Studies on the Genus Biomphalaria-The Intermediate Snail Host of Schistosoma mansoni. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24054895"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.3201\/eid1411.080479","article-title":"Establishment of Biomphalaria tenagophila Snails in Europe","volume":"14","author":"Majoros","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_5","unstructured":"Malek, E.A. (1985). Snail Hosts of Schistosomiasis and Other Snail-Transmitted Diseases in Tropical America: A Manual, Pan American Health Organization."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2225","DOI":"10.1093\/oxfordjournals.molbev.a003769","article-title":"Evolutionary Relationships and Biogeography of Biomphalaria (Gastropoda: Planorbidae) with Implications Regarding Its Role as Host of the Human Bloodfluke, Schistosoma mansoni","volume":"18","author":"DeJong","year":"2001","journal-title":"Mol. Biol. Evol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1111\/j.1096-3642.2007.00330.x","article-title":"Phylogeny and Biogeography of African Biomphalaria (Gastropoda: Planorbidae), with Emphasis on Endemic Species of the Great East African Lakes","volume":"151","author":"Jorgensen","year":"2007","journal-title":"Zool. J. Linn. Soc."},{"key":"ref_8","first-page":"345","article-title":"The Endemiology and Epidemiology of Schistosomiasis in the Sudan","volume":"36","author":"Archibald","year":"1933","journal-title":"J. Trop. Med. Hyg."},{"key":"ref_9","unstructured":"Manjing, B.K. (1978). Snail Population Fluctuations In-Relation to Schistosoma mansoni Transmission in Gezira Irrigated. [Master\u2019s Thesis, Universty of Khartoum]."},{"key":"ref_10","unstructured":"Hilali, A.H. (1992). Transmission of Schistosoma mansoni in the Managil Area. [Master\u2019s Thesis, University of Khartoum]."},{"key":"ref_11","first-page":"57","article-title":"Focality and Seasonality of Schistosoma mansoni Transmission in the Gezira Irrigated Area, Sudan","volume":"88","author":"Babiker","year":"1985","journal-title":"J. Trop. Med. Hyg."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"853","DOI":"10.2307\/2403751","article-title":"Distribution of Freshwater Snails in Irrigation Schemes in the Sudan","volume":"25","author":"Madsen","year":"1988","journal-title":"J. Appl. Ecol."},{"key":"ref_13","unstructured":"Osman, A. (2012). Snails\u2019 Population Dynamics and Their Parasitic Infections with Trematode in Barakat Canal, Gezira Scheme) 2011. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_14","unstructured":"Hassan, R. (2016). Distribution, Ecological Factors of Snail Species and Their Infection with Trematodes in Wadrabiaa Area, Almadina Arab Administration Unit, South Gezira Locality, Gezira State, Sudan. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira, Sudan University of Gezira]."},{"key":"ref_15","unstructured":"Musa, H. (2016). Distribution, Ecological Factors and Trematode Infectivity of Snails Al Madia Arab, South Gezira Locality, Gezira State, Sudan. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_16","unstructured":"Edris, S. (2017). Distribution, Ecological Factors and Trematode Infectivity of Snails in New Halfa Locality, Kassala State, Sudan. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_17","unstructured":"Hommed, M. (2017). Seasonality, Ecological Factors of Snail Species and their Infection with Trematode in Almosna Canal, New Halfa Locality, Kassala State, Sudan. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_18","unstructured":"Apdelpagi, W. (2017). Studies on Freshwater Snails Distribution, Identification and their Infection with Cercaria in Elfaw Locality Gadarif State. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_19","unstructured":"Harron, D. (2015). Situation Analysis of Schistosomaiasis in Umshoka Unit, Singa Locality, Sinner State. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_20","unstructured":"Elbasheer, A. (2017). Distribution, Ecological Factors and Trematode Infectivity of Snails in Algetaina Locality, White Nile State, Sudan. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_21","unstructured":"Mohieldeen, N. (2017). Seasonality, Ecological Factors of Snail Species and their Infection with Trematodes in Gandtw Area, Shendi Locality, River Nile State, Sudan. [Master\u2019s Thesis, Blue Nile National Institute for Communicable Diseases, University of Gezira]."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1186\/s13071-019-3689-z","article-title":"Epidemiological Findings and Policy Implications from the Nationwide Schistosomiasis and Intestinal Helminthiasis Survey in Sudan","volume":"12","author":"Cha","year":"2019","journal-title":"Parasites Vectors"},{"key":"ref_23","unstructured":"Boelee, E., and Madsen, H. (2006). Irrigation and Schistosomiasis in Africa: Ecological Aspects, IWMI."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Ghiselli, F., Gomes-Dos-Santos, A., Adema, C.M., Lopes-Lima, M., Sharbrough, J., and Boore, J.L. (2021). Molluscan Mitochondrial Genomes Break the Rules. Philos. Trans. R. Soc. Lond. B Biol. Sci., 376.","DOI":"10.1098\/rstb.2020.0159"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Grande, C., Templado, J., and Zardoya, R. (2008). Evolution of Gastropod Mitochondrial Genome Arrangements. BMC Evol. Biol., 8.","DOI":"10.1186\/1471-2148-8-61"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1093\/genetics\/138.2.423","article-title":"Complete DNA Sequence of the Mitochondrial Genome of the Black Chiton, Katharina tunicata","volume":"138","author":"Boore","year":"1994","journal-title":"Genetics"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"baab056","DOI":"10.1093\/database\/baab056","article-title":"MODB: A Comprehensive Mitochondrial Genome Database for Mollusca","volume":"2021","author":"Qu","year":"2021","journal-title":"Database"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0378-1119(99)00270-X","article-title":"Evolutionary Genomics in Metazoa: The Mitochondrial DNA as a Model System","volume":"238","author":"Saccone","year":"1999","journal-title":"Gene"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1046\/j.1365-294X.2003.02063.x","article-title":"The Incomplete Natural History of Mitochondria","volume":"13","author":"Ballard","year":"2004","journal-title":"Mol. Ecol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Tao, K., Gao, Y., Yin, H., Liang, Q., Yang, Q., and Yu, X. (2024). Comparative Mitogenome Analyses of Fifteen Ramshorn Snails and Insights into the Phylogeny of Planorbidae (Gastropoda: Hygrophila). Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25042279"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"4975","DOI":"10.1007\/s11033-020-05541-0","article-title":"Genetic Diversity of Biomphalaria pfeifferi, the Intermediate Host of Schistosoma mansoni in Shamva District, Zimbabwe: Role on Intestinal Schistosomiasis Transmission","volume":"47","author":"Zhou","year":"2020","journal-title":"Mol. Biol. Rep."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Bu, L., Lu, L., Laidemitt, M.R., Zhang, S.-M., Mutuku, M., Mkoji, G., Steinauer, M., and Loker, E.S. (2023). A Genome Sequence for Biomphalaria pfeifferi, the Major Vector Snail for the Human-Infecting Parasite Schistosoma mansoni. PLoS Neglected Trop. Dis., 17.","DOI":"10.1371\/journal.pntd.0011208"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1080\/00034983.2001.11813664","article-title":"Spatio-Temporal Genetic Variability in the Schistosome Intermediate Host Biomphalaria pfeifferi","volume":"95","author":"Webster","year":"2001","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1038\/sj.hdy.6800127","article-title":"Genetic Differentiation, Dispersal and Mating System in the Schistosome-Transmitting Freshwater Snail Biomphalaria glabrata","volume":"89","author":"Pointier","year":"2002","journal-title":"Heredity"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1086\/343875","article-title":"A Spatial and Temporal Approach to Microevolutionary Forces Affecting Population Biology in the Freshwater Snail Biomphalaria pfeifferi","volume":"160","author":"Charbonnel","year":"2002","journal-title":"Am. Nat."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2213","DOI":"10.1046\/j.1365-294X.2002.01586.x","article-title":"The Influence of Mating System, Demography, Parasites and Colonization on the Population Structure of Biomphalaria pfeifferi in Madagascar","volume":"11","author":"Charbonnel","year":"2002","journal-title":"Mol. Ecol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1080\/00034983.2001.11813630","article-title":"Population Genetics of the Schistosome Intermediate Host Biomphalaria pfeifferi in the Zimbabwean Highveld: Implications for Co-Evolutionary Theory","volume":"95","author":"Webster","year":"2001","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Andrus, P.S., Stothard, J.R., and Wade, C.M. (2023). Seasonal Patterns of Schistosoma mansoni Infection within Biomphalaria Snails at the Ugandan Shorelines of Lake Albert and Lake Victoria. PLoS Neglected Trop. Dis., 17.","DOI":"10.1371\/journal.pntd.0011506"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1017\/S0031182000006831","article-title":"Phylogenetic Relationships among Brazilian Biomphalaria Species (Mollusca: Planorbidae) Based upon Analysis of Ribosomal ITS2 Sequences","volume":"121","author":"Vidigal","year":"2000","journal-title":"Parasitology"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2351","DOI":"10.1098\/rspb.2000.1291","article-title":"Molecular Evidence Supports an African Affinity of the Neotropical Freshwater Gastropod, Biomphalaria glabrata, Say 1818, an Intermediate Host for Schistosoma mansoni","volume":"267","author":"Campbell","year":"2000","journal-title":"Proc. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s40249-018-0505-5","article-title":"Morphological and Molecular Characterization of Invasive Biomphalaria straminea in Southern China","volume":"7","author":"Habib","year":"2018","journal-title":"Infect. Dis. Poverty"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1080\/01650521.2023.2225236","article-title":"Integrative Taxonomy and Revision of the Neotropical Biomphalaria tenagophila (Mollusca: Planorbidae) Complex Taxa","volume":"59","author":"Ohlweiler","year":"2023","journal-title":"Stud. Neotrop. Fauna Environ."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3897\/zookeys.668.10562","article-title":"Molecular and Morphological Identification of Biomphalaria Species from the State of S\u00e3o Paulo, Brazil","volume":"668","author":"Palasio","year":"2017","journal-title":"ZooKeys"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1080\/15627020.2008.11407404","article-title":"Sympatric Biomphalaria Species (Gastropoda: Planorbidae) in Lake Albert, Uganda, Show Homoplasies in Shell Morphology","volume":"43","author":"Plam","year":"2008","journal-title":"Afr. Zool."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1186\/s13071-014-0524-4","article-title":"The Population Genetic Structure of Biomphalaria choanomphala in Lake Victoria, East Africa: Implications for Schistosomiasis Transmission","volume":"7","author":"Standley","year":"2014","journal-title":"Parasites Vectors"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Alharbi, M.H., Condemine, C., Hesketh, J., Kayuni, S.A., Arme, T.M., Archer, J., Jones, S., LaCourse, E.J., Makaula, P., and Musaya, J. (2023). Biomphalaria Pfeifferi (Gastropoda: Planorbidae) in Lake Malawi and Upper Shire River, Mangochi District, Malawi: Distribution, Genetic Diversity and Pre-Patent Schistosome Infections. Trop. Med. Infect. Dis., 8.","DOI":"10.3390\/tropicalmed8020126"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/S0168-9525(01)02272-7","article-title":"Molecular Phylogenetics: State-of-the-Art Methods for Looking into the Past","volume":"17","author":"Whelan","year":"2001","journal-title":"Trends Genet."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1645\/GE-284R","article-title":"The Mitochondrial Genome of Biomphalaria glabrata (Gastropoda: Basommatophora), Intermediate Host of Schistosoma mansoni","volume":"90","author":"Dejong","year":"2004","journal-title":"J. Parasitol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.ympev.2010.05.026","article-title":"Conservation and Variation in Mitochondrial Genomes of Gastropods Oncomelania hupensis and Tricula hortensis, Intermediate Host Snails of Schistosoma in China","volume":"57","author":"Zhao","year":"2010","journal-title":"Mol. Phylogenetics Evol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"100017","DOI":"10.1016\/j.crpvbd.2021.100017","article-title":"Mitochondrial Genome of Bulinus truncatus (Gastropoda: Lymnaeoidea): Implications for Snail Systematics and Schistosome Epidemiology","volume":"1","author":"Young","year":"2021","journal-title":"Curr. Res. Parasitol. Vector-Borne Dis."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Zhang, S.-M., Bu, L., Laidemitt, M.R., Lu, L., Mutuku, M.W., Mkoji, G.M., and Loker, E.S. (2018). Complete Mitochondrial and rDNA Complex Sequences of Important Vector Species of Biomphalaria, Obligatory Hosts of the Human-Infecting Blood Fluke, Schistosoma mansoni. Sci. Rep., 8.","DOI":"10.1038\/s41598-018-25463-z"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Pennance, T., Calvelo, J., Tennessen, J.A., Burd, R., Cayton, J., Bollmann, S.R., Blouin, M.S., Spaan, J.M., Hoffmann, F.G., and Ogara, G. (2024). 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 Genom., 25.","DOI":"10.1186\/s12864-024-10103-w"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1590\/S0074-02762010000400027","article-title":"Phylogenetic Analysis of Biomphalaria tenagophila (Orbigny, 1835) (Mollusca: Gastropoda)","volume":"105","author":"Ruiz","year":"2010","journal-title":"Mem\u00f3rias do Instituto Oswaldo Cruz"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1080\/23802359.2019.1579060","article-title":"The Complete Mitochondrial Genome of Invasive Species Biomphalaria straminea (Planorbidae: Biomphalaria) and Phylogenetic Analysis","volume":"4","author":"Zhou","year":"2019","journal-title":"Mitochondrial DNA Part B"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.pt.2006.02.008","article-title":"The Snail (Biomphalaria glabrata) Genome Project","volume":"22","author":"Raghavan","year":"2006","journal-title":"Trends Parasitol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"15451","DOI":"10.1038\/ncomms15451","article-title":"Whole Genome Analysis of a Schistosomiasis-Transmitting Freshwater Snail","volume":"8","author":"Adema","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Zhong, D., Bu, L., Habib, M.R., Lu, L., Yan, G., and Zhang, S.-M. (2024). A Haplotype-like, Chromosome-Level Assembled and Annotated Genome of Biomphalaria glabrata, an Important Intermediate Host of Schistosomiasis and the Best Studied Model of Schistosomiasis Vector Snails. PLoS Neglected Trop. Dis., 18.","DOI":"10.1371\/journal.pntd.0011983"},{"key":"ref_58","first-page":"giac012","article-title":"Genome of the Ramshorn Snail Biomphalaria straminea\u2014An Obligate Intermediate Host of Schistosomiasis","volume":"11","author":"Nong","year":"2022","journal-title":"GigaScience"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1080\/23802359.2018.1503939","article-title":"The Mitochondrial Genome of the Planorbid Snail Planorbella duryi","volume":"3","author":"Schultz","year":"2018","journal-title":"Mitochondrial DNA B Resour."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1016\/S0959-437X(98)80035-X","article-title":"Big Trees from Little Genomes: Mitochondrial Gene Order as a Phylogenetic Tool","volume":"8","author":"Boore","year":"1998","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Hassell, E., Kim, T., and Park, J.-K. (2020). The Mitochondrial Genome in Nematode Phylogenetics. Front. Ecol. Evol., 8.","DOI":"10.3389\/fevo.2020.00250"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1038\/hdy.2008.62","article-title":"Evolution of the Mitochondrial Genome of Metazoa as Exemplified by Comparison of Congeneric Species","volume":"101","author":"Gissi","year":"2008","journal-title":"Heredity"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1073\/pnas.48.4.582","article-title":"On the Genetic Basis of Variation and Heterogeneity of DNA Base Composition","volume":"48","author":"Sueoka","year":"1962","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1089\/omi.2006.10.119","article-title":"Requirements and Standards for Organelle Genome Databases","volume":"10","author":"Boore","year":"2006","journal-title":"Omics"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/S0168-9525(97)01118-9","article-title":"Strand Asymmetries in DNA Evolution","volume":"13","author":"Francino","year":"1997","journal-title":"Trends Genet."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1186\/s13071-022-05308-5","article-title":"Correction: The Complete Mitochondrial Genomes of Paradiplozoon yarkandense and Paradiplozoon homoion Confirm That Diplozoidae Evolve at an Elevated Rate","volume":"15","author":"Hao","year":"2022","journal-title":"Parasites Vectors"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"103961","DOI":"10.1016\/j.meegid.2019.103961","article-title":"The Complete Mitochondrial Genome of Echinostoma miyagawai: Comparisons with Closely Related Species and Phylogenetic Implications","volume":"75","author":"Li","year":"2019","journal-title":"Infect. Genet. Evol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.meegid.2016.01.010","article-title":"The Complete Mitochondrial Genome of Metorchis orientalis (Trematoda: Opisthorchiidae): Comparison with Other Closely Related Species and Phylogenetic Implications","volume":"39","author":"Na","year":"2016","journal-title":"Infect. Genet. Evol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.gene.2013.09.077","article-title":"Evolution of the tRNA Gene Family in Mitochondrial Genomes of Five Meretrix Clams (Bivalvia, Veneridae)","volume":"533","author":"Wu","year":"2014","journal-title":"Gene"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.gene.2012.08.037","article-title":"A Unique tRNA Gene Family and a Novel, Highly Expressed ORF in the Mitochondrial Genome of the Silver-Lip Pearl Oyster, Pinctada maxima (Bivalvia: Pteriidae)","volume":"510","author":"Wu","year":"2012","journal-title":"Gene"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Feng, J., Guo, Y., Yan, C., Ye, Y., Li, J., Guo, B., and L\u00fc, Z. (2020). Comparative Analysis of the Complete Mitochondrial Genomes in Two Limpets from Lottiidae (Gastropoda: Patellogastropoda): Rare Irregular Gene Rearrangement within Gastropoda. Sci. Rep., 10.","DOI":"10.1038\/s41598-020-76410-w"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"10543","DOI":"10.1093\/nar\/gkz833","article-title":"Improved Annotation of Protein-Coding Genes Boundaries in Metazoan Mitochondrial Genomes","volume":"47","author":"Donath","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Standley, C.J., Wade, C.M., and Stothard, J.R. (2011). A Fresh Insight into Transmission of Schistosomiasis: A Misleading Tale of Biomphalaria in Lake Victoria. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0026563"},{"key":"ref_74","first-page":"88","article-title":"Prevalence of Intestinal and Urinary Schistosomaisis in Five Localities in Gezira State, Sudan","volume":"2","author":"Talha","year":"2018","journal-title":"Int. J. Med. Sci. Health Res."},{"key":"ref_75","unstructured":"WHO (2017). Field Use of Molluscicides in Schistosomiasis Control Programmes: An Operational Manual for Programme Managers, WHO."},{"key":"ref_76","first-page":"169","article-title":"Large-Scale Assessment of the Molluscicides Copper Sulphate and N-Tritlymorpholine (Frescon) in the North Group of the Gezira Irrigated Area, Sudan","volume":"75","author":"Amin","year":"1972","journal-title":"J. Trop. Med. Hyg."},{"key":"ref_77","unstructured":"Danish Bilharziasis Laboratory (1998). Danish Bilharziasis Laboratory WHO a Field Guide to African Freshwater Snails, WHO collaborating Centre for Applied Malacology."},{"key":"ref_78","unstructured":"Frandsen, F., McCullough, F., Madsen, H., World Health Organization, and Danish Bilharziasis Lab (1980). A Practical Guide to the Identification of African Freshwater Snails, Danish Bilharziasis Lab. No. 1\u20132."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Bhat, A.I., and Rao, G.P. (2020). Rolling Circle Amplification (RCA). Characterization of Plant Viruses: Methods and Protocols, Springer.","DOI":"10.1007\/978-1-0716-0334-5"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1186\/s13148-016-0287-1","article-title":"cPAS-Based Sequencing on the BGISEQ-500 to Explore Small Non-Coding RNAs","volume":"8","author":"Fehlmann","year":"2016","journal-title":"Clin. Epigenetics"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"Fastp: An Ultra-Fast All-in-One FASTQ Preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_82","unstructured":"Andrews, S. (2025, May 08). FastQC: A Quality Control Tool for High Throughput Sequence Data. Available online: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_83","first-page":"e18","article-title":"NOVOPlasty: De Novo Assembly of Organelle Genomes from Whole Genome Data","volume":"45","author":"Dierckxsens","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"e63","DOI":"10.1093\/nar\/gkz173","article-title":"MitoZ: A Toolkit for Animal Mitochondrial Genome Assembly, Annotation and Visualization","volume":"47","author":"Meng","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1093\/bioinformatics\/btm573","article-title":"ARWEN: A Program to Detect tRNA Genes in Metazoan Mitochondrial Nucleotide Sequences","volume":"24","author":"Laslett","year":"2008","journal-title":"Bioinformatics"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"9077","DOI":"10.1093\/nar\/gkab688","article-title":"tRNAscan-SE 2.0: Improved Detection and Functional Classification of Transfer RNA Genes","volume":"49","author":"Chan","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: Molecular Evolutionary Genetics Analysis Version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"3299","DOI":"10.1093\/molbev\/msx248","article-title":"DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets","volume":"34","author":"Rozas","year":"2017","journal-title":"Mol. Biol. Evol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.2144\/00286ir01","article-title":"The Sequence Manipulation Suite: JavaScript Programs for Analyzing and Formatting Protein and DNA Sequences","volume":"28","author":"Stothard","year":"2000","journal-title":"Biotechniques"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1016\/j.molp.2023.09.010","article-title":"TBtools-II: A \u201cOne for All, All for One\u201d Bioinformatics Platform for Biological Big-Data Mining","volume":"16","author":"Chen","year":"2023","journal-title":"Mol. Plant"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: Multiple Sequence Alignment with High Accuracy and High Throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML Version 8: A Tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies","volume":"30","author":"Stamatakis","year":"2014","journal-title":"Bioinformatics"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4756\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:33:37Z","timestamp":1760031217000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4756"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,16]]},"references-count":92,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["ijms26104756"],"URL":"https:\/\/doi.org\/10.3390\/ijms26104756","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2025,5,16]]}}}