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Molecular detection of piroplasmids in mammals from the Superorder Xenarthra in Brazil

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Abstract

Xenarthra mammals can be found from southern North America to southern South America, including all Brazilian biomes. Although it has been shown that Xenarthra mammals can play a role as reservoirs for several zoonotic agents, few studies investigate the diversity of piroplasmids (Apicomplexa: Piroplasmida) in this group of mammals. Taking into account that piroplasmids can cause disease in animals and humans, understanding the prevalence and diversity of piroplasmids in Xenarthra mammals would contribute to conservation efforts for this group of animals as well as to infer risk areas for transmission of emergent zoonosis. The present study aimed to investigate the occurrence and molecular identity of piroplasmids in free-living mammals of the Superorder Xenarthra from four Brazilian states (Mato Grosso do Sul, São Paulo, Rondônia, and Pará). For this, DNA was extracted from blood or spleen samples from 455 animals. A nested PCR based on the 18S rRNA gene was used as screening for piroplasmids. Of the 455 samples analyzed, 25 (5.5%) were positive. Additionally, PCR assays based on 18S rRNA near-complete, cox-1, cox-3, hsp70, cytB, β-tubulin genes and the ITS-1 intergenic region were performed. Five out of 25 positive samples also tested positive for ITS-1-based PCR. The phylogenetic analysis positioned three 18S rRNA sequences detected in Priodontes maximus into the same clade of Babesia sp. detected in marsupials (Didelphis albiventris, Didelphis marsupialis, and Monodelphis domestica) and Amblyomma dubitatum collected from opossums and coatis in Brazil. On the other hand, the 18S rRNA sequence obtained from Dasypus novemcinctus was closely related to a Theileria sp. sequence previously detected in armadillos from Mato Grosso State, grouping in a subclade within the Theileria sensu stricto clade. In the phylogenetic analysis based on the ITS-1 region, the sequences obtained from Myrmecophaga tridactyla and Tamandua tetradactyla were placed into a single clade, apart from the other piroplasmid clades. The present study demonstrated the molecular occurrence of Piroplasmida in anteaters and Babesia sp. and Theileria sp. in armadillos from Brazil.

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Data availability

The datasets generated and analyzed during the current study are available in the NCBI GenBank Nucleotide platform (https://www.ncbi.nlm.nih.gov/genbank/) and can be accessed through accession numbers OQ969878-OQ969881 and OQ974563-OQ974565.

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Acknowledgements

The authors would like to thank “Laboratório de Filogenia e Taxonomia Molecular de Tripanossomatídeos” Institute of Biology (IB) Institute of Biomedical Sciences (ICB), USP (São Paulo, SP, Brazil), ICAS (Instituto de Conservação de Animais Silvestres - Projeto Bandeiras e Rodovias e Projeto de Conservação do Tatu-Canastra), and Wildlife Pathology Service of the School of Agricultural and Veterinarian Sciences.

Funding

This work was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado da São Paulo - Process #2020/12037-0) and CNPq (National Council for Scientific and Technological Development; Productivity Grant to MRA [CNPq Process #303701/2021-8]). A.C.C. and P.V.C.A. were supported by FAPESP (2020/07826-5; 2021/00353-7).

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Conceptualization: Ana Cláudia Calchi and Marcos Rogério André; Methodology: Ana Cláudia Calchi, Débora Regina Yogui, Mario Henrique Alves, Arnaud Leonard Jean Desbiez, Danilo Kluyber, Juliana Gaboardi Vultão, Paulo Vitor Cadina Arantes, Mariele de Santi, Karin Werther, and Marta Maria Geraldes Teixeira; Writing – original draft preparation: Ana Cláudia Calchi, Débora Regina Yougui, Mario Henrique Alves, Arnaud Leonard Jean Desbiez, Danilo Kluyber, Juliana Gaboardi Vultão, Mariele de Santi, Paulo Vitor Cadina Arantes, Karin Werther, Marta Maria Geraldes Teixeira, Rosangela Zacarias Machado, and Marcos Rogério André; Writing -review and editing: Ana Cláudia Calchi and Marcos Rogério André; Funding acquisition: Marcos Rogério André; Supervision: Marcos Rogério André.

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Correspondence to Marcos Rogério André.

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Ethical approval

Animal procedures and management protocols were approved by Institute Chico Mendes for Conservation of Biodiversity (SISBIO number 53798–5) and by the Ethics Committees on Animal use of the ICB—USP (protocol number 98) and the School of Agricultural and Veterinarian Sciences (FCAV/UNESP) (protocol number 9412/2022). The DNA samples were registered under SISGEN #A4C38D5 (“Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado”).

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Calchi, A.C., Yogui, D.R., Alves, M.H. et al. Molecular detection of piroplasmids in mammals from the Superorder Xenarthra in Brazil. Parasitol Res 122, 3169–3180 (2023). https://doi.org/10.1007/s00436-023-08008-w

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  • DOI: https://doi.org/10.1007/s00436-023-08008-w

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