Abstract
Wild rodent species are naturally infected by Schistosoma mansoni; however, the genetic characterization of the parasite, its parasitological features, and its role in human schistosomiasis are poorly understood. In this study, we isolated and characterized Schistosoma from naturally infected Holochilus sciureus, called HS strain, collected from a schistosomiasis endemic region in Maranhão State, Brazil. To isolate the parasite, miracidia obtained from the livers of H. sciureus were used to infect Biomphalaria glabrata of sympatric (called SB) and allopatric (called BH) strains, and the produced cercariae were subcutaneously inoculated into hamsters and/or BALB/c mice. Parasitological kinetics in experimentally infected hosts were evaluated, and the tRNACys-12S (referred to as 16S herein) and cox 1 regions of mtDNA from isolated worms were amplified and sequenced. Only miracidia obtained from infected mice, but not from hamsters, were capable of infecting B. glabrata, allowing maintenance of the isolated parasite. Cox1 and 16S mtDNA sequences showed 100% similarity with S. mansoni, and phylogenetic analysis showed that the HS strain of S. mansoni forms an assemblage with isolates from America and Kenya, confirming the conspecificity. Experimental infection of B. glabrata SB with S. mansoni HS resulted in two peaks of cercariae shedding at 45 and 70 days post-infection (dpi) and caused higher mortality than in B. glabrata BH. The worm recovery rate in mice was approximately 13%, and the peak of egg elimination occurred at the 10th week post-infection. Therefore, S. mansoni obtained from H. sciureus was successfully isolated, genetically characterized, and maintained in mice, allowing further study of this schistosome strain.
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Acknowledgements
We would like to thank Universidade Estadual do Maranhão (UEMA) for supplying transportation and laboratory infrastructure for conducting the field research. We are also grateful for the assistance of Sr. Zé da Boroca, Davi Viegas Melo, and Gleycka Carvalho Gomes during rodent sampling in the municipality of São Bento. Finally, we thank Elizabeth De Lacorte for technical support provided to care for and breed our experimental models.
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DN-C received research fellowship from Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq- Brazil). GSM received a fellowship and support from Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA-Brazil, grant number BD-02007/19). The funders had no role in the study design, data collection, and analysis, or in the decision to publish the manuscript.
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Guilherme Silva Miranda and Deborah A. Negrão-Corrêa: Conceptualization, field collection, performed experiments, molecular analysis, data analysis, supervision and project administration, and writing and editing the original draft. João Gustavo Mendes Rodrigues: field collection, performed experiments, and edited the original draft; Neuton Silva-Souza: Field collection and performed experiments. Samira Diniz Resende, Genil Mororó Araújo Camelo, Jeferson K.A.O. Silva, and José Carlos Reis: Performed experiments and edited original draft. Luis Fernando Viana Furtado, Elida Mara Leite Rabelo, and Felipe Bisaggio Pereira: Molecular analysis and edited the original draft. All the authors reviewed and approved the final version of this manuscript.
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The capture of H. sciureus was authorized by the Biodiversity Authorization and Information System (n°67253–1) and the project is registered in the National System for the Management of Genetic Heritage and Associated Traditional Knowledge (registration number AB9E2EC). The experimental procedures were approved by the Ethics Committee on Animal Use of the State University of Maranhão (UEMA, Brazil; protocol nº03/2017) and of the Federal University of Minas Gerais (UFMG, Brazil; protocols nº46/2019 and nº368/2018).
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Miranda, G.S., Rodrigues, J.G.M., Resende, S.D. et al. From field to laboratory: isolation, genetic assessment, and parasitological behavior of Schistosoma mansoni obtained from naturally infected wild rodent Holochilus sciureus (Rodentia, Cricetidae), collected in Northeastern Brazil. Parasitol Res 122, 395–411 (2023). https://doi.org/10.1007/s00436-022-07710-5
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DOI: https://doi.org/10.1007/s00436-022-07710-5