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Apicomplexans in small mammals from Chile, with the first report of the Babesia microti group in South American rodents

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Abstract

Small mammals play an essential role as disseminators of pathogens because they reach high population densities and have ubiquitous distributions. In the Northern Hemisphere rodents are well recognized as reservoirs for tick-borne bacteria of the Anaplasmataceae family and also apicomplexan protozoans. In contrast, South American rodents hosting these microorganisms have been rarely identified. In this study, we collected blood from rodents and marsupials in northern Chile and screened for Anaplasmataceae bacteria and apicomplexan protozoa. Overall, 14.7% of the samples were positive for Babesia, Hepatozoon, and Sarcocystidae using conventional PCR assays targeting the structural 18S rRNA locus (18S). Phylogenetic analyses performed with amplicons derived from 18S and cytochrome c oxidase (COI) gene provided evidence of a Babesia sp. belonging to the Babesia microti group in Phyllotis darwini, and a novel Babesia genotype in P. darwini and Abrothrix jelskii. Furthermore, four novel genotypes of Hepatozoon retrieved from Abrothrix olivacea, P. darwini, and Oligoryzomys longicaudatus, formed independent lineages within a clade that includes additional Hepatozoon spp. detected in South American rodents. Moreover, an incidental finding of a previously detected apicomplexan, herein designated as Sarcocystidae sp., was recorded in Thylamys opossums with a high prevalence, indicating a possible specific association with these mammals. Phylogenetic analysis of Sarcoystidae sp. clearly demonstrated its relatedness to apicomplexans detected in Australian marsupials. Our results expand the range of mammals hosting tick-borne apicomplexans in South America, highlight a novel clade consisting of South American babesias, and report for the first time the B. microti group infecting rodents in the region.

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Acknowledgements

We thank Constanza Aguilera, Angel Oviedo, Ignacio Troncoso, and Juan Uribe for their collaboration in field and laboratory work. To Dr. Jonas Moraes-Filho for providing positive controls to perform genetic screenings. To Dr. Douglas McIntosh for kindly providing advice on English language. This paper is dedicated to the memory of Dr. Daniel González-Acuña, who made significant contributions to the study of parasites in Chile and passed away while this study was being elaborated.

Funding

This study was supported by the “Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT)” N° 1170972 and by the ANID BECAS/Scholarship Program/DOCTORADO NACIONAL/2019–21190078 and 2020–21200182. Funders had no role in the study design, data collection, analysis, preparation of the manuscript, and decision to publish it.

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Adriana M. Santodomingo: conceptualization, data curation, methodology, formal analysis, investigation, writing—original draft, and writing—review and editing. Richard S. Thomas: conceptualization, formal analysis, investigation, methodology, and writing—review and editing. Julian F. Quintero-Galvis: formal analysis, methodology, and review and editing. Diana M. Echeverry-Berrio: methodology, writing—original draft, and writing—review and editing. María C. Silva-de la Fuente: methodology, and review and editing. Lucila Moreno-Salas: formal analysis, investigation, project administration, review and editing. Sebastián Muñoz-Leal: conceptualization, data curation, methodology, resources, formal analysis, investigation, project administration, writing—original draft, and writing—review and editing. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sebastián Muñoz-Leal.

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Ethics approval

Procedures performed in this study were verified and approved by the Bioethics Committee of School of Veterinary Sciences, Universidad de Concepción (Form CBE-19–2017). Captures of small mammals and field work in national parks and reserves were authorized by the Servicio Agrícola y Ganadero (SAG; Resolution No. 1532/2019 and 9071/2018), and the Corporación Nacional Forestal (CONAF; Permits 39/2018; 67/2019; 05/2018; 76/2018; 66/2018), respectively.

Competing interests

The authors declare no competing interests.

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Handling Editor: Una Ryan

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Santodomingo, A.M., Thomas, R.S., Quintero-Galvis, J.F. et al. Apicomplexans in small mammals from Chile, with the first report of the Babesia microti group in South American rodents. Parasitol Res 121, 1009–1020 (2022). https://doi.org/10.1007/s00436-022-07452-4

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  • DOI: https://doi.org/10.1007/s00436-022-07452-4

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