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Evidence and molecular characterization of Bartonella spp. and hemoplasmas in neotropical bats in Brazil

  • P. IKEDA (a1), M. C. SEKI (a2), A. O. T. CARRASCO (a2), L. V. RUDIAK (a2), J. M. D. MIRANDA (a2), S. M. M. GONÇALVES (a2), E. G. L. HOPPE (a1), A. C. A. ALBUQUERQUE (a3), M. M. G. TEIXEIRA (a4), C. E. PASSOS (a1), K. WERTHER (a1), R. Z. MACHADO (a1) and M. R. ANDRÉ (a1)...


The order Chiroptera is considered the second largest group of mammals in the world, hosting important zoonotic virus and bacteria. Bartonella and hemotropic mycoplasmas are bacteria that parasite different mammals’ species, including humans, causing different clinical manifestations. The present work aimed investigating the occurrence and assessing the phylogenetic positioning of Bartonella spp. and Mycoplasma spp. in neotropical bats sampled from Brazil. Between December 2015 and April 2016, 325 blood and/or tissues samples were collected from 162 bats comprising 19 different species sampled in five states of Brazil. Out of 322 bat samples collected, while 17 (5·28%) were positive to quantitative PCR for Bartonella spp. based on nuoG gene, 45 samples (13·97%) were positive to cPCR assays for hemoplasmas based on 16S rRNA gene. While seven sequences were obtained for Bartonella (nuoG) (n = 3), gltA (n = 2), rpoB (n = 1), ftsZ (n = 1), five 16S rRNA sequences were obtained for hemoplasmas. In the phylogenetic analysis, the Bartonella sequences clustered with Bartonella genotypes detected in bats sampled in Latin America countries. All five hemoplasmas sequences clustered together as a monophyletic group by Maximum Likelihood and Bayesian Inference analyses. The present work showed the first evidence of circulation of Bartonella spp. and hemoplasmas among bats in Brazil.

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Corresponding author

*Author for correspondence: M. R. André, Laboratório de Imunoparasitologia, Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias Júlio de Mesquita Filho (UNESP), Campus de Jaboticabal, Via de Acesso Prof. Paulo Donato Castellane, s/n, Zona Rural, CEP: 14884-900, Jaboticabal, São Paulo, Brazil. (Email:


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1. Schipper, J, et al. The status of the world's land and marine mammals: diversity, threat, and knowledge. Science 2008; 322: 255–230. doi: 10.1126/science.1165115.
2. Mühldorfer, K. Bats and bacterial pathogens: a review. Zoonoses and Public Health 2013; 60: 93103. doi: 10.1111/j.1863-2378.2012.01536.x.
3. Morse, SF, et al. Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae). Infection, Genetics and Evolution 2012; 12: 17171723. doi: 10.1016/j.meegid.2012.06.009.
4. Kosoy, M, et al. Bartonella spp. in bats, Kenya. Emerging Infectious Diseases 2010; 16: 18751881. doi: 10.3201/eid1612.100601.
5. Pitassi, LH, et al. Bartonella spp. Bacteremia in Blood Donors from Campinas, Brazil. PLoS Neglected Tropical Diseases 2015; 9(1).
6. Vieira-Damiani, G, et al. Bartonella clarridgeiae bacteremia detected in an asymptomatic blood donor. Journal of Clinical Microbiology 2015; 53: 352356. doi: 10.1128/JCM.00934-14.
7. Euzéby, JP. List of bacterial names with standing in nomenclature: a folder available on the Internet (list of prokaryotic names with standing in nomenclature. International Journal of Systematic Bacteriology 1997; 47: 590592. doi: 10.1099/00207713-47-2-590.
8. Neimark, H, et al. Proposal to transfer some members of the genera Haemobartonella and Eperythozoon to the genus Mycoplasma with descriptions of ‘Candidatus Mycoplasma haemofelis’, ‘Candidatus Mycoplasma haemomuris’, ‘Candidatus Mycoplasma haemosuis’ and ‘Candidatus Mycoplasma wenyonii’. International Journal of Systematic and Evolutionary Microbiology 2001; 51: 891899. doi: 10.1099/00207713-51-3-891.
9. Biondo, AW, et al. A review of the occurrence of hemoplasmas (hemotrophic mycoplasmas) in Brazil. Revista Brasileira de Parasitologia Veterinária (Online) [Online] 2009; 18: 17 doi: 10.4322/rbpv.01803001.
10. Tasker, S. Clinical review: haemotropic mycoplasmas what's their real significance in cats? Journal of Feline Medicine and Surgery 2010; 12: 369381. doi: 10.1016/j.jfms.2010.03.011.
11. dos Santos, AP, et al. Hemoplasma infection in HIV-positive patient, Brazil. Emerging Infectious Diseases 2008; 14: 19221924. doi: 10.3201/eid1412.080964.
12. Mascarelli, P, et al. Hemotropic mycoplasmas in little brown bats (Myotis lucifugus). Parasites & Vectors 2014; 7:117. doi: 10.1186/1756-3305-7-117.
13. Millán, J, et al. Widespread infection with hemotropic mycoplasmas in bats in Spain, including a hemoplasma closely related to “Candidatus Mycoplasma hemohominis”. Comparative Immunology, Microbiology and Infectious Diseases 2015; 39: 912. doi: 10.1016/j.cimid.2015.01.002.
14. Breitschwerdt, EB, et al. Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. Journal of Veterinary Emergency and Critical Care 2010; 20: 830. doi: 10.1111/j.1476-4431.2009.00496.x.
15. Guimarães, AM, et al. Detection of Bartonella spp. in neotropical felids and evaluation of risk factors and hematological abnormalities associated with infection. Veterinary Microbiology 2010; 142: 346351. doi: 10.1016/j.vetmic.2009.10.002.
16. André, MR, et al. Hemoplasmas in wild canids and felids in Brazil. Journal of Zoo and Wildlife Medicine 2011; 42: 342347. doi:10.1638/2010-0198.1.
17. Fleischman, DA, et al. Bartonella clarridgeiae and Bartonella vinsonii subsp. berkhoffii exposure in captive wild canids in Brazil. Epidemiology & Infection 2014; 143: 573577. doi: 10.1017/S0950268814001277.
18. Grazziotin, AL, et al. Prevalence and molecular characterization of Mycoplasma ovis in selected free-ranging Brazilian deer populations. Journal of Wildlife Diseases 2011; 47: 10051011. doi: 10.7589/0090-3558-47.4.1005.
19. Castro, AMMG, et al. Swine infectious agents in Tayassu pecari and Pecari tajacu tissue samples from Brazil. Journal of Wildlife Diseases 2014; 50: 205209. doi: 10.7589/2013-01-021.
20. Santos, LC, et al. Hemotropic mycoplasma in a free-ranging black howler monkey (Alouatta caraya) in Brazil. Journal of Wildlife Diseases 2013; 49: 728731. doi: 10.7589/2012-06-159.
21. Bonato, L, et al. Occurrence and molecular characterization of Bartonella spp. and hemoplasmas in neotropical primates from Brazilian Amazon. Comparative Immunology, Microbiology and Infectious Diseases 2015; 42: 1520. doi: 10.1016/j.cimid.2015.09.001.
22. Vieira, RF, et al. Detection of a novel hemoplasma based on 16S rRNA gene DNA in captive and free-ranging capybaras (Hydrochaeris hydrochaeris). Veterinary Microbiology 2009; 139: 410413. doi: 10.1016/j.vetmic.2009.06.018.
23. Conrado, FO, et al. Occurrence and identification of hemotropic mycoplasmas (Hemoplasmas) in free ranging and laboratory rats (Rattus norvegicus) from two Brazilian zoos. BMC Veterinary Research 2015; 11:286. doi: 10.1186/s12917-015-0601-8.
24. Favacho, AR, et al. Zoonotic Bartonella species in wild rodents in the state of Mato Grosso do Sul, Brazil. Microbes and Infection 2015; 17: 889892. doi: 10.1016/j.micinf.2015.08.014.
25. Gonçalves, LR, et al. Diversity and molecular characterization of novel hemoplasmas infecting wild rodents from different Brazilian biomes. Comparative Immunology, Microbiology and Infectious Diseases 2015; 43: 5056. doi: 10.1016/j.cimid.2015.10.006.
26. Gonçalves, LR, et al. Association of Bartonella species with wild and synanthropic rodents in different Brazilian biomes. Applied and Environmental Microbiology 2016; 82: 71547164. doi: 10.1128/AEM.02447-16.
27. Concannon, R, et al. Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology 2005; 131: 489496. doi: 10.1017/S0031182005008097.
28. Lin, JW, et al. Identification of novel Bartonella spp. in bats and evidence of Asian gray shrew as a new potential reservoir of Bartonella. Veterinary Microbiology 2012; 156: 119126. doi: 10.1016/j.vetmic.2011.09.031.
29. Bai, Y, et al. Prevalence and diversity of Bartonella spp. in bats in Peru. American Journal of Tropical Medicine and Hygiene 2012; 87: 518523. doi: 10.4269/ajtmh.2012.12-0097.
30. Kamani, J, et al. Bartonella species in bats (Chiroptera) and bat flies (Nycteribiidae) from Nigeria, West Africa. Vector-Borne and Zoonotic Diseases 2014; 14: 625–32. doi: 10.1089/vbz.2013.1541.
31. Olival, KJ, et al. Bartonella spp. in a Puerto Rican bat community. Journal of Wildlife Diseases 2015; 51: 274278. doi: 10.7589/2014-04-113.
32. Lilley, TM, Veikkolainen, V, Pulliainen, AT. Molecular detection of ‘Candidatus Bartonella hemsundetiensis’ in bats. Vector-Borne and Zoonotic Disease 2015; 15: 706708. doi: 10.1089/vbz.2015.1783.
33. Brook, CE, et al. Bartonella spp. in Fruit Bats and Blood-Feeding Ectoparasites in Madagascar. PLOS Neglected Tropical Diseases 2015; 10(2). doi: 10.1371/journal.pntd.0003532.
34. Judson, SD, Frank, HK, Hadly, EA. Bartonellae are prevalent and diverse in Costa Rican bats and bat flies. Zoonoses Public Health 2015; 62: 609617. doi: 10.1111/zph.12188.
35. Bai, Y, et al. Bartonella spp. in bats, Guatemala. Emerging Infectious Diseases 2011; 17: 12691272. doi: 10.3201/eid1707.101867.
36. Wray, AK, et al. Viral Diversity, Prey Preference, and Bartonella Prevalence in Desmodus rotundus in Guatemala. EcoHealth 2016; 13:761774. doi: 10.1007/s10393-016-1183-z.
37. Davoust, B, et al. Evidence of Bartonella spp. in blood and ticks (Ornithodoros hasei) of Bats, in French Guiana. Vector-Borne and Zoonotic Diseases 2016; 16: 516519. doi: 10.1089/vbz.2015.
38. Mannerings, AO, et al. Exposure to bat-associated Bartonella spp. among humans and other animals, Ghana. Emerging Infectious Diseases 2016; 22: 922924. doi: 10.3201/eid2205.151908.
39. Leulmi, H, et al. Detection of Bartonella tamiae, Coxiella burnetii and rickettsiae in arthropods and tissues from wild and domestic animals in northeastern Algeria. Parasites & Vectors 2016; 9:27. doi: 10.1186/s13071-016-1316-9.
40. Dietrich, M, et al. Diversity of Bartonella and Rickettsia spp. in bats and their blood-feeding ectoparasites from South Africa and Swaziland. PLoS ONE 2016; 11(3). doi: 10.1371/journal.pone.0152077.
41. Kunz, TH, Kurta, A. Capture methods and holding devices. In: Kunz, TH, ed. Ecological and Behavioural Methods for the Study of Bats. Washington/London: Smithsonian Institution Press, 1988, pp. 129.
42. Peracchi, AL, Nogueira, MR. Lista anotada dos morcegos do Estado do Rio de Janeiro, sudeste do Brasil. Chiroptera Neotropical 2010; 16: 508519.
43. Birkenheuer, AJ, Levy, MG, Breitschwerdt, EB. Development and evaluation of a seminested PCR for detection and differentiation of Babesia gibsoni (Asian genotype) and B. canis DNA in canine blood samples. Journal of Clinical Microbiology 2003; 41: 41724177. doi: 10.1128/JCM.41.9.4172-4177.2003.
44. André, MR, et al. Assessment of a quantitative 5′ nuclease real-time polymerase chain reaction using the nicotinamide adenine dinucleotide dehydrogenase gamma subunit (nuoG) for Bartonella species in domiciled and stray cats in Brazil. Journal of Feline Medicine and Surgery 2015; 18: 783790. doi: 10.1177/1098612X15593787.
45. Bustin, SA, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. American Association of Clinical Chemists 2009; 55: 611622. doi: 10.1373/clinchem.2008.112797.
46. Colborn, JM, et al. Improved detection of Bartonella DNA in mammalian hosts and arthropod vectors by real-time PCR using the NADH dehydrogenase gamma subunit (nuoG). American Society for Microbiology 2010; 48: 46304633. doi: 10.1128/JCM.00470-10.
47. Johnson, G, et al. Detection and identification of Bartonella species pathogenic for humans by PCR amplification targeting the riboflavin synthase gene (ribC). Journal of Clinical Microbiology 2003; 41: 10691072. doi: 10.1128/JCM.41.3.1069-1072.2003.
48. Norman, AF, et al. Differentiation of Bartonella-like isolates at the species level by PCR restriction fragment length polymorphism in the citrate synthase gene. Journal of Clinical Microbiology 1995; 33: 17971803.
49. Paziewska, A, et al. Recombination within and between species of the alpha proteobacterium Bartonella infecting rodents. International Society for Microbial Ecology 2011; 61: 134145. doi: 10.1007/s00248-010-9735-1.
50. Maggi, RG, Breitschwerdt, EB. Potential limitations of the 16S-23S rRNA intergenic region for molecular detection of Bartonella species. Journal of Clinical Microbiology 2005; 43: 11711176. doi: 10.1128/JCM.43.3.1171-1176.2005.
51. Zeaiter, Z, et al. Phylogenetic classification of Bartonella species by comparing groEL sequences. International Journal of Systematic and Evolutionary Microbiology 2002; 52: 165171. doi: 10.1099/00207713-52-1-165.
52. Maggi, RG, Breitschwerdt, EB. Isolation of bacteriophages from Bartonella vinsonii subsp. berkhoffii and the characterization of pap-31 gene sequences from bacterial and phage DNA. Journal of Molecular Microbiology and Biotechnology 2005; 9: 4451. doi: 10.1159/000088145.
53. Maggi, RG, et al. Novel hemotropic Mycoplasma species in white-tailed deer (Odocoileus virginianus). Comparative Immunology, Microbiology and Infectious Diseases 2013; 36: 607611. doi: 10.1016/j.cimid.2013.08.001.
54. Miceli, NG, et al. Molecular detection of feline arthropod-borne pathogens in cats in Cuiabá, state of Mato Grosso, central-western region of Brazil. Revista Brasileira de Parasitologia Veterinária 2013; 23: 385390. doi: 10.1590/S1984-29612013000300011.
55. Sanger, F, Nicklen, S, Coulson, AR. DNA sequencing with chain terminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America 1977; 74(12): 54635467.
56. Ewing, GB, Green, P. Base calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 1998; 8: 186194. doi: 10.1101/gr.8.3.186.
57. Ewing, B, et al. Base calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research 1998; 8: 175185. doi: 10.1101/gr.8.3.175.
58. Altschul, SF, et al. Basic local alignment search tool. Journal of Molecular Biology 1990; 215: 403410. doi: 10.1016/S0022-2836(05)80360-2.
59. Benson, DA, et al. GenBank. Nucleic Acids Research 2013; 41:D37-D42. doi: 10.1093/nar/gks1070.
60. Thompson, JD, Higgins, DG, Gibson, TJ. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 1994; 22: 16734680.
61. Hall, TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999; 41: 9598.
62. Ronquist, F, Huelsenbeck, JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19: 15721574. doi: 10.1093/bioinformatics/btg180.
63. Miller, MA, Pfeiffer, W, Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees In Proceedings of the Gateway Computing Environments Workshop (GCE), 2010, pp. 0108.
64. Trifinopoulos, J, et al. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 2016; 44:W232W235. doi: 10.1093/nar/gkw256.
65. Nguyen, LT, et al. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 2015; 32: 268274. doi: 10.1093/molbev/msu300.
66. Darriba, D, et al. ModelTest 2: more models, new heuristics and parallel computing. Nature Methods 2012; 9: 772. doi: 10.1038/nmeth.2109.
67. Posada, D, Buckley, TR. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 2004; 53: 793808. doi: 10.1080/10635150490522304.
68. Stover, BC, Muller, KF. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 2010; 11: 0109. doi: 10.1186/1471-2105-11-7.
69. Gutiérrez, R, et al. Guidelines for the isolation, molecular detection, and characterization of Bartonella species. Vector Borne Zoonotic Diseases 2017; 17: 4250. doi: 10.1089/vbz.2016.1956.
70. Mckee, CD, et al. Phylogenetic and geographic patterns of Bartonella host shifts among bat species. Infection, Genetics and Evolution 2016; 44: 382394. doi: 10.1016/j.meegid.2016.07.033.
71. Lei, BR, Olival, KJ. Contrasting Patterns in Mammal-Bacteria Coevolution: Bartonella and Leptospira in Bats and Rodents. PLoS Neglected Tropical Diseases 2014; 8(3). doi: 10.1371/journal.pntd.0002738.
72. Steer, JA, et al. A novel hemotropic Mycoplasma (hemoplasma) in a patient with hemolytic anemia and pyrexia. Clinical Infectious Diseases 2011; 53: 147151. doi: 10.1093/cid/cir666.



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