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Molecular detection of Trypanosoma (Trypanosomatidae) in bats from Thailand, with their phylogenetic relationships

Published online by Cambridge University Press:  04 February 2022

Elizabeth Riana
Affiliation:
Veterinary Parasitology Research Unit, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand The International Graduate Program of Veterinary Science and Technology (VST), Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand
Apinya Arnuphapprasert
Affiliation:
Veterinary Parasitology Research Unit, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand Veterinary Pathobiology Graduate Program, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand
Duriyang Narapakdeesakul
Affiliation:
Veterinary Parasitology Research Unit, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand Veterinary Pathobiology Graduate Program, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand
Thongchai Ngamprasertwong
Affiliation:
Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, Thailand
Monsicha Wangthongchaicharoen
Affiliation:
Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, Thailand
Pipat Soisook
Affiliation:
Princess Maha Chakri Sirindhorn Natural History Museum, Prince of Songkla University, Songkhla, Thailand Harrison Institute, Bowerwood House, No. 15, St Botolph's Road, Sevenoaks, Kent TN13 3AQ, UK
Phanaschakorn Bhodhibundit
Affiliation:
Sai Yok National Park, Department of National Parks, Wildlife and Plant Conservation, Kanchanaburi, Thailand
Morakot Kaewthamasorn*
Affiliation:
Veterinary Parasitology Research Unit, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand
*
Author for correspondence: Morakot Kaewthamasorn, E-mail: [email protected]

Abstract

The vast majority of trypanosome species is vector-borne parasites, with some of them being medically and veterinary important (such as Trypanosoma cruzi and Trypanosoma brucei) and capable of causing serious illness in vertebrate hosts. The discovery of trypanosomes in bats emphasizes the importance of bats as an important reservoir. Interestingly, there is a hypothesis that bats are ancestral hosts of T. cruzi. Trypanosome diversity has never been investigated in bats in Thailand, despite being in a biodiversity hot spot. To gain a better understanding of the diversity and evolutionary relationship of trypanosomes, polymerase chain reaction-based surveys were carried out from 2018 to 2020 in 17 sites. A total of 576 bats were captured, representing 23 species. A total of 38 (6.6%) positive samples was detected in ten bat species. Trypanosoma dionisii and Trypanosoma noyesi were identified from Myotis siligorensis and Megaderma spasma, respectively. The remaining 18S rRNA sequences of trypanosomes were related to other trypanosomes previously reported elsewhere. The sequences in the current study showed nucleotide identity as low as 90.74% compared to those of trypanosomes in the GenBank database, indicating the possibility of new species. All bat trypanosomes identified in the current study fall within the T. cruzi clade. The current study adds to evidence linking T. noyesi to a bat trypanosome and further supports the bat host origin of the T. cruzi clade. To the best of authors' knowledge, this is the first study on bat trypanosomes in Thailand and their phylogenetic relationships with global isolates.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Acosta, Ida C, Da Costa, AP, Gennari, SM and Marcili, A (2014) Survey of Trypanosoma and Leishmania in Wild and Domestic Animals in an Atlantic Rainforest Fragment and Surroundings in the State of Espírito Santo, Brazil. Journal of Medical Entomology 51, 686693.CrossRefGoogle Scholar
Arnuphapprasert, A, Riana, E, Ngamprasertwong, T, Wangthongchaicharoen, M, Soisook, P, Thanee, S, Bhodhibundit, P and Kaewthamasorn, M (2020) First molecular investigation of haemosporidian parasites in Thai bat species. International Journal for Parasitology: Parasites and Wildlife 13, 5161.Google ScholarPubMed
Austen, J and Barbosa, A (2021) Diversity and epidemiology of bat trypanosomes: a One Health perspective. Pathogens 10, 126.CrossRefGoogle ScholarPubMed
Austen, JM, Van Kampen, E, Egan, SL, O'Dea, MA, Jackson, B, Ryan, UM, Irwin, PJ and Prada, D (2020) First report of Trypanosoma dionisii (Trypanosomatidae) identified in Australia. Parasitology 147, 18011809.CrossRefGoogle ScholarPubMed
Baker, JR (1973) First European record of Trypanosoma (Megatrypanum) sp. of bats. Nature New Biology 241, 9696.CrossRefGoogle ScholarPubMed
Barbosa, AD, Mackie, JT, Stenner, R, Gillett, A, Irwin, P and Ryan, U (2016) Trypanosoma teixeirae: a new species belonging to the T. cruzi clade causing trypanosomosis in an Australian little red flying fox (Pteropus scapulatus). Veterinary Parasitology 223, 214221.CrossRefGoogle Scholar
Barros, JHS, Lima, L, Schubach, AO and Teixeira, MMG (2019) Trypanosoma madeirae sp. n.: a species of the clade T. cruzi associated with the neotropical common vampire bat Desmodus rotundus. International Journal for Parasitology: Parasites and Wildlife 8, 7181.Google Scholar
Bergner, LM, Becker, DJ, Tello, C, Carrera, JE and Streicker, DG (2021 a) Detection of Trypanosoma cruzi in the saliva of diverse neotropical bats. Zoonoses and Public Health 68, 271276. https://doi.org/10.1111/zph.12808CrossRefGoogle ScholarPubMed
Bergner, LM, Mollentze, N, Orton, RJ, Tello, C, Broos, A, Biek, R and Streicker, DG (2021 b) Characterizing and evaluating the zoonotic potential of novel viruses discovered in vampire bats. Viruses 13, 118. doi: 10.3390/v13020252CrossRefGoogle ScholarPubMed
Bevans, AI, Fitzpatrick, DM, Stone, DM, Butler, BP, Smith, MP and Cheetham, S (2020) Phylogenetic relationships and diversity of bat-associated Leptospira and the histopathological evaluation of these infections in bats from Grenada, West Indies. PLoS Neglected Tropical Diseases 14, e0007940.CrossRefGoogle ScholarPubMed
Bogitsh, BJ, Carter, CE and Oeltmann, TN (2019). Chapter 18 – Arthropods as vectors. In Bogitsh, BJ, Carter, CE and Oeltmann, TN (eds), Human Parasitology. New York, USA: Academic Press, pp. 331360.CrossRefGoogle Scholar
Botero, A, Cooper, C, Thompson, CK, Clode, PL, Rose, K and Thompson, RCA (2016) Morphological and phylogenetic description of Trypanosoma noyesi sp. nov.: an Australian wildlife trypanosome within the T. cruzi clade. Protist 167, 425439.CrossRefGoogle ScholarPubMed
Cai, Y, Wang, X, Zhang, N, Li, J, Gong, P, He, B and Zhang, X (2019) First report of the prevalence and genotype of Trypanosoma spp. in bats in Yunnan Province, Southwestern China. Acta Tropica 198, 105105.CrossRefGoogle ScholarPubMed
Calisher, CH, Childs, JE, Field, HE, Holmes, KV and Schountz, T (2006) Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19, 531545.CrossRefGoogle ScholarPubMed
Cavazzana, M, Marcili, A, Lima, L, da Silva, FM, Junqueira, ÂCV, Veludo, HH, Viola, LB, Campaner, M, Nunes, VLB, Paiva, F, Coura, JR, Camargo, EP and Teixeira, MMG (2010) Phylogeographical, ecological and biological patterns shown by nuclear (ssrRNA and gGAPDH) and mitochondrial (Cyt b) genes of trypanosomes of the subgenus Schizotrypanum parasitic in Brazilian bats. International Journal for Parasitology 40, 345355.CrossRefGoogle ScholarPubMed
Chen, S-F, Shen, T-J, Lee, H-C, Wu, H-W, Zeng, W-T, Lu, D-J and Lin, H-C (2017) Preference of an insular flying fox for seed figs enhances seed dispersal of a dioecious species. Biotropica 49, 511520.CrossRefGoogle Scholar
Chernomor, O, von Haeseler, A and Minh, BQ (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65, 9971008.CrossRefGoogle ScholarPubMed
Clément, L, Dietrich, M, Markotter, W, Fasel, NJ, Monadjem, A, López-Baucells, A, Scaravelli, D, Théou, P, Pigeault, R, Ruedi, M and Christe, P (2020) Out of Africa: the origins of the protozoan blood parasites of the Trypanosoma cruzi clade found in bats from Africa. Molecular Phylogenetics and Evolution 145, 106705.CrossRefGoogle ScholarPubMed
Dario, MA, Rodrigues, MS, Barros, JHDS, Xavier, SCDC, D'Andrea, PS, Roque, ALR and Jansen, AM (2016) Ecological scenario and Trypanosoma cruzi DTU characterization of a fatal acute Chagas disease case transmitted orally (Espírito Santo state, Brazil). Parasites & Vectors 9, 477.CrossRefGoogle Scholar
Dario, MA, Lisboa, CV, Costa, LM, Moratelli, R, Nascimento, MP, Costa, LP, Leite, YLR, Llewellyn, MS, Xavier, SCdC, Roque, ALR and Jansen, AM (2017) High Trypanosoma spp. diversity is maintained by bats and triatomines in Espírito Santo state, Brazil. PloS One 12, e0188412. doi: 10.1371/journal.pone.0188412CrossRefGoogle Scholar
Descloux, E, Mediannikov, O, Gourinat, A-C, Colot, J, Chauvet, M, Mermoud, I, Desoutter, D, Cazorla, C, Klement-Frutos, E, Antonini, L, Levasseur, A, Bossi, V, Davoust, B, Merlet, A, Goujart, M-A, Oedin, M, Brescia, F, Laumond, S, Fournier, P-E and Raoult, D (2021) Flying fox hemolytic fever, description of a new zoonosis caused by Candidatus Mycoplasma haemohominis. Clinical Infectious Diseases 73, e1445e1453.CrossRefGoogle ScholarPubMed
Dos Santos, FCB, Lisboa, CV, Xavier, SCC, Dario, MA, Verde, RS, Calouro, AM, Roque, ALR and Jansen, AM (2018) Trypanosoma sp. diversity in Amazonian bats (Chiroptera; Mammalia) from Acre State, Brazil. Parasitology 145, 828837.CrossRefGoogle ScholarPubMed
Dumonteil, E, Elmayan, A, Majeau, A, Tu, W, Duhon, B, Marx, P, Wolfson, W, Balsamo, G and Herrera, C (2020) Genetic diversity of Trypanosoma cruzi parasites infecting dogs in southern Louisiana sheds light on parasite transmission cycles and serological diagnostic performance. PLoS Neglected Tropical Diseases 14, e0008932.CrossRefGoogle ScholarPubMed
Esch, K and Petersen, C (2013) Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clinical Microbiology Reviews 26, 5885.CrossRefGoogle ScholarPubMed
Espinosa-Álvarez, O, Ortiz, PA, Lima, L, Costa-Martins, AG, Serrano, MG, Herder, S, Buck, GA, Camargo, EP, Hamilton, PB, Stevens, JR and Teixeira, MMG (2018) Trypanosoma rangeli is phylogenetically closer to Old World trypanosomes than to Trypanosoma cruzi. International Journal for Parasitology 48, 569584.CrossRefGoogle ScholarPubMed
Fan, Y, Zhao, K, Shi, Z-L and Zhou, P (2019) Bat coronaviruses in China. Viruses 11, 114. doi: 10.3390/v11030210CrossRefGoogle ScholarPubMed
Francis, CM (2008) A Field Guide to the Mammals of Thailand and South-East Asia. Bangkok: Asia Books.Google Scholar
Gardner, RA and Molyneux, DH (1988 a) Schizotrypanum in British bats. Parasitology 97, 4350.CrossRefGoogle ScholarPubMed
Gardner, RA and Molyneux, DH (1988 b) Trypanosoma (Megatrypanum) incertum from Pipistrellus pipistrellus: development and transmission by cimicid bugs. Parasitology 96, 433447.CrossRefGoogle ScholarPubMed
Haag, J, O'HUigin, C and Overath, P (1998) The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 3749.CrossRefGoogle ScholarPubMed
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series, vol. 41, pp. 9598.Google Scholar
Hamilton, PB, Stevens, JR, Gaunt, MW, Gidley, J and Gibson, WC (2004) Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 13931404.CrossRefGoogle ScholarPubMed
Hamilton, PB, Gibson, WC and Stevens, JR (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Molecular Phylogenetics and Evolution 44, 1525.CrossRefGoogle ScholarPubMed
Hamilton, PB, Adams, ER, Njiokou, F, Gibson, WC, Cuny, G and Herder, S (2009) Phylogenetic analysis reveals the presence of the Trypanosoma cruzi clade in African terrestrial mammals. Infection, Genetics and Evolution 9, 8186.CrossRefGoogle ScholarPubMed
Hamilton, PB, Cruickshank, C, Stevens, JR, Teixeira, MMG and Mathews, F (2012 a) Parasites reveal movement of bats between the New and Old worlds. Molecular Phylogenetics and Evolution 63, 521526.CrossRefGoogle ScholarPubMed
Hamilton, PB, Teixeira, MMG and Stevens, JR (2012 b) The evolution of Trypanosoma cruzi: the ‘bat seeding’ hypothesis. Trends in Parasitology 28, 136141.CrossRefGoogle ScholarPubMed
Hoare, CA (1966) The classification of mammalian trypanosomes. In Henle, W, Kikuth, W, Meyer, KF, Nauck, EG and Tomcsik, J (eds), Ergebnisse der Mikrobiologie Immunitätsforschung und Experimentellen Therapie: Fortsetzung der Ergebnisse der Hygiene Bakteriologie Immunitätsforschung und Experimentellen Therapie Begründet von Wolfgang Weichardt. Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 4357.CrossRefGoogle Scholar
Hoare, CA (1972) The Trypanosomes of Mammals. A Zoological Monograph. Oxford: Blackwell Scientific Publications Ltd.Google Scholar
Hodo, CL, Goodwin, CC, Mayes, BC, Mariscal, JA, Waldrup, KA and Hamer, SA (2016) Trypanosome species, including Trypanosoma cruzi, in sylvatic and peridomestic bats of Texas, USA. Acta Tropica 164, 259266.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle ScholarPubMed
Kessler, MK, Becker, DJ, Peel, AJ, Justice, NV, Lunn, T, Crowley, DE, Jones, DN, Eby, P, Sánchez, CA and Plowright, RK (2018) Changing resource landscapes and spillover of henipaviruses. Annals of the New York Academy of Sciences 1429, 7899. https://doi.org/10.1111/nyas.13910.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Kunz, TH, Braun de Torrez, E, Bauer, D, Lobova, T and Fleming, TH (2011) Ecosystem services provided by bats. Annals of the New York Academy of Sciences, 1223, 138.CrossRefGoogle ScholarPubMed
Lanfear, R, Calcott, B, Ho, SYW and Guindon, S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 16951701.CrossRefGoogle ScholarPubMed
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772773.Google ScholarPubMed
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 11101116.CrossRefGoogle Scholar
Lemos, M, Fermino, BR, Simas-Rodrigues, C, Hoffmann, L, Silva, R, Camargo, EP, Teixeira, MMG and Souto-Padrón, T (2015) Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species. Parasites & Vectors 8, 573.CrossRefGoogle Scholar
Letko, M, Seifert, SN, Olival, KJ, Plowright, RK and Munster, VJ (2020) Bat-borne virus diversity, spillover and emergence. Nature Reviews Microbiology 18, 461471.CrossRefGoogle ScholarPubMed
Lima, L, Silva, FMD, Neves, L, Attias, M, Takata, CSA, Campaner, M, de Souza, W, Hamilton, PB and Teixeira, MMG (2012) Evolutionary insights from bat trypanosomes: morphological, developmental and phylogenetic evidence of a new species, Trypanosoma (Schizotrypanum) erneyi sp. nov., in African bats closely related to Trypanosoma (Schizotrypanum) cruzi and allied species. Protist 163, 856872.CrossRefGoogle ScholarPubMed
Lima, L, Espinosa-Álvarez, O, Hamilton, PB, Neves, L, Takata, CSA, Campaner, M, Attias, M, de Souza, W, Camargo, EP and Teixeira, MMG (2013) Trypanosoma livingstonei: a new species from African bats supports the bat seeding hypothesis for the Trypanosoma cruzi clade. Parasites & Vectors 6, 221221.CrossRefGoogle ScholarPubMed
Lima, L, Espinosa-Álvarez, O, Pinto, CM, Cavazzana, M Jr, Pavan, AC, Carranza, JC, Lim, BK, Campaner, M, Takata, CSA, Camargo, EP, Hamilton, PB and Teixeira, MMG (2015) New insights into the evolution of the Trypanosoma cruzi clade provided by a new trypanosome species tightly linked to Neotropical Pteronotus bats and related to an Australian lineage of trypanosomes. Parasites & Vectors, 8, 657.CrossRefGoogle Scholar
Loftis, AD, Gill, JS, Schriefer, ME, Levin, ML, Eremeeva, ME, Gilchrist, MJR and Dasch, GA (2005) Detection of Rickettsia, Borrelia, and Bartonella in Carios kelleyi (Acari: Argasidae). Journal of Medical Entomology 42, 473480.Google Scholar
Mafie, E, Rupa, FH, Takano, A, Suzuki, K, Maeda, K and Sato, H (2018) First record of Trypanosoma dionisii of the T. cruzi clade from the eastern bent-winged bat (Miniopterus fuliginosus) in the Far East. Parasitology Research 117, 673680.CrossRefGoogle Scholar
Maia da Silva, F, Marcili, A, Lima, L, Cavazzana, M, Ortiz, PA, Campaner, M, Takeda, GF, Paiva, F, Nunes, VLB, Camargo, EP and Teixeira, MMG (2009). Trypanosoma rangeli isolates of bats from central Brazil: genotyping and phylogenetic analysis enable description of a new lineage using spliced-leader gene sequences. Acta Tropica, 109, 199207.CrossRefGoogle ScholarPubMed
Maiguashca Sánchez, J, Sueto, SOB, Schwabl, P, Grijalva, MJ, Llewellyn, MS and Costales, JA (2020) Remarkable genetic diversity of Trypanosoma cruzi and Trypanosoma rangeli in two localities of southern Ecuador identified via deep sequencing of mini-exon gene amplicons. Parasites & Vectors 13, 252.CrossRefGoogle ScholarPubMed
Majeau, A, Murphy, L, Herrera, C and Dumonteil, E (2021) Assessing Trypanosoma cruzi parasite diversity through comparative genomics: implications for disease epidemiology and diagnostics. Pathogens 10, 212.CrossRefGoogle ScholarPubMed
Marinkelle, CJ (1982) Developmental stages of Trypanosoma cruzi-like flagellates in Cavernicola pilosa. Revista de Biología Tropical 30, 107111.Google ScholarPubMed
McInnes, LM, Gillett, A, Ryan, UM, Austen, J, Campbell, RSF, Hanger, J and Reid, SA (2009) Trypanosoma irwini n. sp (Sarcomastigophora: Trypanosomatidae) from the koala (Phascolarctos cinereus). Parasitology 136, 875885.CrossRefGoogle Scholar
McInnes, LM, Hanger, J, Simmons, G, Reid, SA and Ryan, UM (2011) Novel trypanosome Trypanosoma gilletti sp. (Euglenozoa: Trypanosomatidae) and the extension of the host range of Trypanosoma copemani to include the koala (Phascolarctos cinereus). Parasitology 138, 5970.CrossRefGoogle Scholar
Molyneux, D (1991) Trypanosomes of bats. In Kreier, J and Baker, J (eds), Parasitic Protozoa, vol. 1. San Diego: Academic Press. pp. 195223.Google Scholar
Murray, K, Selleck, P, Hooper, P, Hyatt, A, Gould, A, Gleeson, L, Westbury, H, Hiley, L, Selvey, L, Rodwell, B and Ketterer, P (1995) A morbillivirus that caused fatal disease in horses and humans. Science 268, 9497.CrossRefGoogle ScholarPubMed
Nawata, E, Nagata, Y, Sasaki, A, Iwama, K and Sakuratani, T (2005) Mapping of climatic data in northeast Thailand: rainfall. Tropics 14, 191201.CrossRefGoogle Scholar
Nguyen, L-T, Schmidt, HA, von Haeseler, A and Minh, BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268274.CrossRefGoogle ScholarPubMed
Noyes, HA, Stevens, JR, Teixeira, M, Phelan, J and Holz, P (1999) A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331339.CrossRefGoogle ScholarPubMed
Noyes, HA, Stevens, JR, Teixeira, M, Phelan, J and Holz, P (2000) Corrigendum to ‘A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia’. [International Journal for Parasitology 29 (2) (1999) 331–339]. International Journal for Parasitology 30, 228.CrossRefGoogle Scholar
Ortiz-Baez, AS, Cousins, K, Eden, JS, Chang, WS, Harvey, E, Pettersson, JH, Carver, S, Polkinghorne, A, Šlapeta, J, Rose, K and Holmes, EC (2020) Meta-transcriptomic identification of Trypanosoma spp. in native wildlife species from Australia. Parasites & Vectors 13, 447.CrossRefGoogle ScholarPubMed
Phumee, A, Tawatsin, A, Thavara, U, Pengsakul, T, Thammapalo, S, Depaquit, J, Gay, F and Siriyasatien, P (2017) Detection of an unknown Trypanosoma DNA in a Phlebotomus stantoni (Diptera: Psychodidae) collected from southern Thailand and records of new sand flies with reinstatement of Sergentomyia hivernus Raynal & Gaschen, 1935 (Diptera: Psychodidae). Journal of Medical Entomology 54, 429434.Google Scholar
Ponte-Sucre, A (2016) An overview of Trypanosoma brucei infections: an intense host–parasite interaction. Frontiers in Microbiology 7, 112. doi: 10.3389/fmicb.2016.02126CrossRefGoogle ScholarPubMed
Poofery, J, Narapakdeesakul, D, Riana, E, Arnuphapprasert, A, Nugraheni, YR, Ngamprasertwong, T, Wangthongchaicharoen, M, Soisook, P, Bhodhibundit, P and Kaewthamasorn, M (2021) Molecular identification and genetic diversity of Bartonella spp. in 24 bat species from Thailand. Transboundary and Emerging Diseases, 117. doi: https://doi.org/10.1111/tbed.14389Google ScholarPubMed
Qiu, Y, Kajihara, M, Harima, H, Hang'ombe, BM, Nakao, R, Hayashida, K, Mori-Kajihara, A, Changula, K, Eto, Y, Ndebe, J, Yoshida, R, Takadate, Y, Mwizabi, D, Kawabata, H, Simuunza, M, Mweene, A, Sawa, H, Takada, A and Sugimoto, C (2019) Molecular characterization and phylogenetic analysis of Trypanosoma spp. detected from striped leaf-nosed bats (Hipposideros vittatus) in Zambia. International Journal for Parasitology: Parasites and Wildlife 9, 234238.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Systematic Biology 67, 901904.CrossRefGoogle ScholarPubMed
Ramírez, JD, Hernández, C, Montilla, M, Zambrano, P, Flórez, AC, Parra, E and Cucunubá, ZM (2014) First report of human Trypanosoma cruzi infection attributed to TcBat genotype. Zoonoses and Public Health 61, 477479.CrossRefGoogle ScholarPubMed
Rangel, DA, Lisboa, CV, Novaes, RLM, Silva, BA, Souza, RF, Jansen, AM, Moratelli, R and Roque, ALR (2019) Isolation and characterization of trypanosomatids, including Crithidia mellificae, in bats from the Atlantic Forest of Rio de Janeiro, Brazil. PLoS Neglected Tropical Diseases 13, e0007527.CrossRefGoogle ScholarPubMed
Rodrigues, MS, Lima, L, Xavier, S, Herrera, HM, Rocha, FL, Roque, ALR, Teixeira, MMG and Jansen, AM (2019) Uncovering Trypanosoma spp. diversity of wild mammals by the use of DNA from blood clots. International Journal for Parasitology: Parasites and Wildlife 8, 171181.Google ScholarPubMed
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 15721574.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 32993302.CrossRefGoogle ScholarPubMed
Sándor, AD, Mihalca, AD, Domşa, C, Péter, Á and Hornok, S (2021) Argasid ticks of Palearctic bats: distribution, host selection, and zoonotic importance. Frontiers in Veterinary Science 8, 684737. https://doi.org/10.3389/fvets.2021.684737.CrossRefGoogle ScholarPubMed
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671675.CrossRefGoogle ScholarPubMed
Schnittger, L, Yin, H, Gubbels, MJ, Beyer, D, Niemann, S, Jongejan, F and Ahmed, JS (2003) Phylogeny of sheep and goat Theileria and Babesia parasites. Parasitology Research 91, 398406.Google ScholarPubMed
Simmons, NB and Cirranello, AL (2020) Bat Species of the World: A taxonomic and geographic database.Google Scholar
Srisuton, P, Phumee, A, Sunantaraporn, S, Boonserm, R, Sor-Suwan, S, Brownell, N, Pengsakul, T and Siriyasatien, P (2019) Detection of Leishmania and Trypanosoma DNA in field-caught sand flies from endemic and non-endemic areas of Leishmaniasis in Southern Thailand. Insects 10, 111. doi: 10.3390/insects10080238CrossRefGoogle ScholarPubMed
Stevens, J, Noyes, H and Gibson, W (1998) The evolution of trypanosomes infecting humans and primates. Memorias do Instituto Oswaldo Cruz 93, 669676.CrossRefGoogle ScholarPubMed
Stevens, JR, Noyes, HA, Dover, GA, Dover, WC and Gibson, WC (1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107116.CrossRefGoogle ScholarPubMed
Szentiványi, T, Markotter, W, Dietrich, M, Clément, L, Ançay, L, Brun, L, Genzoni, E, Kearney, T, Seamark, E, Estók, P, Christe, P and Glaizot, O (2020) Host conservation through their parasites: molecular surveillance of vector-borne microorganisms in bats using ectoparasitic bat flies. Parasite 27, 110.CrossRefGoogle ScholarPubMed
Szpeiter, BB, Ferreira, J, Assis, FFV, Stelmachtchuk, FN, Peixoto, KDCJ, Ajzenberg, D, Minervino, AHH, Gennari, SM and Marcili, A (2017) Bat trypanosomes from Tapajós-Arapiuns extractive reserve in Brazilian Amazon. Revista Brasileira de Parasitologia Veterinária 26, 17.CrossRefGoogle ScholarPubMed
Takahashi, HG and Yasunari, T (2006) A climatological monsoon break in rainfall over Indochina – a singularity in the seasonal march of the Asian summer monsoon. Journal of Climate 19, 15451556.CrossRefGoogle Scholar
Taylor, M, Clinton, E and Tuttle, MD (2019) Bats: An Illustrated Guide to All Species. London, UK: Ivy Press.Google Scholar
Torres-Castro, M, Cuevas-Koh, N, Hernández-Betancourt, S, Noh-Pech, H, Estrella, E, Herrera-Flores, B, Panti-May, JA, Waleckx, E, Sosa-Escalante, J and Peláez-Sánchez, R (2021) Natural infection with Trypanosoma cruzi in bats captured in Campeche and Yucatán, México. Biomedica: Revista del Instituto Nacional de Salud 41, 131140.CrossRefGoogle ScholarPubMed
Villena, FE, Gomez-Puerta, LA, Jhonston, EJ, Del Alcazar, OM, Maguina, JL, Albujar, C, Laguna-Torres, VA, Recuenco, SE, Ballard, SB and Ampuero, JS (2018) First report of Trypanosoma cruzi infection in salivary gland of bats from the Peruvian Amazon. American Journal of Tropical Medicine and Hygiene 99, 723728.CrossRefGoogle ScholarPubMed
Wang, LJ, Han, HJ, Zhao, M, Liu, JW, Luo, LM, Wen, HL, Qin, XR, Zhou, CM, Qi, R, Yu, H and Yu, XJ (2019) Trypanosoma dionisii in insectivorous bats from northern China. Acta Tropica 193, 124128.CrossRefGoogle ScholarPubMed
Yob, JM, Field, H, Rashdi, AM, Morrissy, C, van der Heide, B, Rota, P, Bin Adzhar, A, White, J, Daniels, P, Jamaluddin, A and Ksiazek, T (2001) Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerging Infectious Diseases 7, 439441.CrossRefGoogle Scholar
Zhou, P, Yang, X-L, Wang, X-G, Hu, B, Zhang, L, Zhang, W, Si, H-R, Zhu, Y, Li, B, Huang, C-L, Chen, H-D, Chen, J, Luo, Y, Guo, H, Jiang, R-D, Liu, M-Q, Chen, Y, Shen, X-R, Wang, X, Zheng, X-S, Zhao, K, Chen, Q-J, Deng, F, Liu, L-L, Yan, B, Zhan, F-X, Wang, Y-Y, Xiao, G-F and Shi, Z-L (2020) A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579, 270273.CrossRefGoogle ScholarPubMed
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