Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T02:43:17.290Z Has data issue: false hasContentIssue false
  • English
  • Français

Trypanosoma sp. diversity in Amazonian bats (Chiroptera; Mammalia) from Acre State, Brazil

Published online by Cambridge University Press:  16 November 2017

Francisco C.B. dos Santos ,
Cristiane V. Lisboa ,
Samanta C.C. Xavier ,
Maria A. Dario ,
Rair de S. Verde ,
Armando M. Calouro ,
André Luiz R. Roque  and
Ana M. Jansen
Francisco C.B. dos Santos
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, CEP 21040-360, Rio de Janeiro/RJ, Brazil Instituto Federal do Acre, Rua Rio Grande do Sul, S/N°, Aeroporto Velho, CEP 69911-036, Rio Branco/AC, Brazil
Cristiane V. Lisboa
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, CEP 21040-360, Rio de Janeiro/RJ, Brazil
Samanta C.C. Xavier
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, CEP 21040-360, Rio de Janeiro/RJ, Brazil
Maria A. Dario
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, CEP 21040-360, Rio de Janeiro/RJ, Brazil
Rair de S. Verde
Affiliation:
Laboratório de Ecologia de Mamíferos, Universidade Federal do Acre, BR 364, Km 04, CEP 69920-900, Rio Branco/AC, Brazil
Armando M. Calouro
Affiliation:
Laboratório de Ecologia de Mamíferos, Universidade Federal do Acre, BR 364, Km 04, CEP 69920-900, Rio Branco/AC, Brazil
André Luiz R. Roque*
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, CEP 21040-360, Rio de Janeiro/RJ, Brazil
Ana M. Jansen
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, CEP 21040-360, Rio de Janeiro/RJ, Brazil
*
Author for correspondence: A.L.R. Roque, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Bats are ancient hosts of Trypanosoma species and their flying ability, longevity and adaptability to distinct environments indicate that they are efficient dispersers of parasites. Bats from Acre state (Amazon Biome) were collected in four expeditions conducted in an urban forest (Parque Zoobotânico) and one relatively more preserved area (Seringal Cahoeira) in Rio Branco and Xapuri municipalities. Trypanosoma sp. infection was detected by hemoculture and fresh blood examination. Isolated parasite species were identified by the similarity of the obtained DNA sequence from 18S rDNA polymerase chain reaction and reference strains. Overall, 367 bats from 23 genera and 32 species were examined. Chiropterofauna composition was specific to each municipality, although Artibeus sp. and Carollia sp. prevailed throughout. Trypanosoma sp. infection was detected in 85 bats (23·2%). The most widely distributed and prevalent genotypes were (in order) Trypanosoma cruzi TcI, T. cruzi marinkellei, Trypanosoma dionisii, T. cruzi TcIV and Trypanosoma rangeli. At least one still-undescribed Trypanosoma species was also detected in this study. The detection of T. cruzi TcI and TcIV (the ones associated with Chagas disease in Amazon biome) demonstrates the putative importance of these mammal hosts in the epidemiology of the disease in the Acre State.

Keywords

Trypanosoma spbatsAmazon BasinTrypanosoma cruziChagas disease
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 828 - 837
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 214–221.CrossRefGoogle Scholar
Bernard, E (2001) Vertical stratification of bat communities in primary forest of Central Amazon, Brazil. Journal of Tropical Ecology 17, 115–126.Google Scholar
Bernard, E, Tavares, VC and Sampaio, E (2011) Compilação atualizada das espécies de morcegos (Chiroptera) para a Amazônia Brasileira. Biota Neotropica 11, 35–46.CrossRefGoogle Scholar
Borghesan, TC, Ferreira, RC, Takata, CS, Campaner, M, Borda, CC, Paiva, F, Milder, RV, Teixeira, MM and Camargo, EP (2013) Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypansomatidae) a genus of insect parasites associated with flies. Protist 164, 129–152.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, 425–439.CrossRefGoogle ScholarPubMed
Burland, TG (2000) DNASTAR's lasergene sequence analysis software. In Misener, S and Krawetz, SA (eds). Bioinformatics Methods and Protocols, vol. 132, Methods in Molecular Biology, Tonada, USA: Humana Press, pp. 71–91.Google Scholar
Carrillo-Araujo, M, Taş, N, Alcántara-Hernández, RJ, Gaona, O, Schondube, JE, Medellín, RA and Falcón, LI (2015) Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies. Frontiers in Microbiology 6, 447.CrossRefGoogle ScholarPubMed
Coura, JR and Junqueira, ACV (2015) Ecological diversity of Trypanosoma cruzi transmission in the Amazon Basin. The main scenaries in the Brazilian Amazon. Acta Tropica 151, 51–57.Google Scholar
Coura, JR, Albajar-Viñas, P and Junqueira, ACV (2014) Ecoepidemiology, short history and control of Chagas disease in the endemic countries and the new challenge for non-endemic countries. Memórias do Instituto Oswaldo Cruz 109, 856–862.Google Scholar
da Costa, AP, Nunes, PH, Leite, BHS, Ferreira, JIGDS, Tonhosolo, R, da Rosa, AR and Marcili, A (2016) Diversity of bats trypanosomes in hydroeletric area of Belo Monte in Brazilian Amazonia. Acta Tropica 164, 185–193.Google Scholar
Dario, MA, Rodrigues, MS, da Silva Barros, JH, das Chagas Xavier, SC, 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
Dechmann, DKN, Kalko, EKV and Kerth, G (2004) Ecology of an exceptional roost: energetic benefits could explain why the bat Lophostoma silvicolum roosts in active termite nests. Evolutionary Ecology Research 6, 1037–1050.Google Scholar
Díaz, MM, Aguirre, LF and Barquez, RM (2011) Clave de Identificación de los Murciélagos del Cono sur de Sudamérica. Cochabamba, Bolivia: Centro de Estudios en Biología Teórica y Aplicada.Google Scholar
Fenton, MB and Simmons, NB (2015) Bats, A World of Science and Mystery. Chicago, USA: The University of Chicago Press.Google Scholar
Garcia, L, Ortiz, S, Osorio, G, Torrico, MC, Torrico, F and Solari, A (2012) Phylogenetic analysis of Bolivian bat trypanosomes of the subgenus Schizotrypanum based on cytochrome B sequence and minicircle analyses. PLoS ONE 7, e36578.CrossRefGoogle ScholarPubMed
Gardner, AL (1979) Feeding habits. In Baker, RJ, Jones, J, Knox, J. and Carter, DC (eds). Biology of Bats of the New World Family Phyllostomatidae. Part II. Lubbock, USA: The Museum Texas Tech University, pp. 293–350.Google Scholar
Gardner, AL (2007) Order Chiroptera. In Gardner, AL (ed.). Mammals of South America: Volume 1 Marsupials, Xenarthrans, Shrews, and Bats. Chicago, USA: University of Chicago Press, pp. 187–498.Google Scholar
Hamilton, PB, Cruickshank, C, Stevens, JR, Teixeira, MMG and Mathews, F (2012) Parasites reveal movement of bats between the new and old worlds. Molecular Phylogenetic Evolution 63, 521–526.CrossRefGoogle ScholarPubMed
Hoorn, C, Wesselingh, FP, Ter Steege, H, Bermudez, MA, Mora, A, Sevink, J and Jaramillo, C (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927–931.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Lima, L, Da Silva, FM, Neves, L, Attias, M, Takata, CS, Campaner, M and Teixeira, MM (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, 856–872.Google Scholar
Lima, L, Espinosa-Álvarez, O, Hamilton, PB, Neves, L, Takata, CS, Campaner, M and Teixeira, MM (2013) Trypanosoma livingstonei: a new species from African bats supports the bat seeding hypothesis for the Trypanosoma cruzi clade. Parasites & Vectors 6, 1.Google Scholar
Lima, L, Espinosa-Alvarez, O, Pinto, CM, Cavazzana, M Jr., Pavan, AC and Carranza, JC (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.Google Scholar
Luis, AD, Hayman, DT, O'Shea, TJ, Cryan, PM, Gilbert, AT, Pulliam, JR, Mills, JN, Timonin, ME, Willis, CK, Cunningham, AA, Fooks, AR, Rupprecht, CE, Wood, JL and Webb, CT (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society B: Biological Sciences 280, 20122753.Google Scholar
Maia da Silva, F, Marcili, A, Lima, L, Cavazzana, M Jr, Ortiz, PA, Campaner, M, Takeda, GF, Paiva, F, Nunes, VL, Camargo, EP and Teixeira, MM (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, 199–207.Google Scholar
Marinkelle, CJ (1976) The biology of the trypanosomes of bats. In Lumdsen, WHR and Evans, DA (eds). Biology of the Kinetoplastida. New York, USA: Academic Press, pp. 175–216.Google Scholar
Molyneux, D. H. (1991) Trypanosomes of bats. In Kreier, JP and Baker, JR (eds). Parasitic Protozoa. London, UK: Academic Press, pp. 195–223.Google Scholar
Noyes, HA, Stevens, JR, Teixeira, M, Phelan, J and Holz, P (1999) A nested PCR for the sssrRNA gene detects Trypanosoma binney in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331–339.CrossRefGoogle Scholar
Ramírez, JD, Hernández, C, Montilla, M, Zambrano, P, Flórez, AC and Parra, E (2014) First report of human Trypanosoma cruzi infection attributed to TcBat genotype. Zoonoses and Public Health 61, 477–479.Google Scholar
R Development Core Team (2010) R: A Language and Environment for Statistical Computing, Reference Index Version 2.11.1 (2010-05-31). Vienna, Austria: The R Foundation for Statistical Computing.Google Scholar
Rojas, D, Vale, A, Ferrero, V and Navarro, L (2011) When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae. Molecular Ecology 20, 2217–2228.Google Scholar
Stoner, KE (2000) Leaf selection by the tent-making bat Artibeus watsoni in Asterogyne martiana Palms in Southwestern Costa Rica. Journal of Tropical Ecology 16, 151–157.Google Scholar
Vallejo, GA, Guhl, F, Chiari, E and Macedo, AM (1999) Species specific detection of Trypanosoma cruzi and Trypanosoma rangeli in vector and mammal hosts by polymerase chain reaction amplification of kinetoplast minicircle DNA. Acta Tropica 72, 203–212.Google Scholar
Wilkinson, GS and South, JM (2002) Life history, ecology and longevity in bats. Aging Cell 1, 124–1131.Google Scholar
Wilkinson, GS, Carter, GG, Bohn, KM and Adams, DM (2016) Non-kin cooperation in bats. Philosophical Transactions of the Royal Society B: Biological Sciences 371, 20150095.Google Scholar
Zingales, B, Miles, MA, Campbell, DA, Tibayrenc, M, Macedo, AM, Teixeira, MMG, Schijman, AG, Llewellyn, MS, Lages-Silva, E, Machado, CR, Andrade, SG and Sturm, NR (2012) The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological, relevance and research applications. Infection, Genetics and Evolution 12, 240–253.CrossRefGoogle ScholarPubMed
Supplementary material: File

dos Santos et al supplementary material

Table S2

Download dos Santos et al supplementary material(File)
File 14.2 KB