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Prevalence and Genetic Diversity of Bartonella Spp. in Northern Bats (Eptesicus nilssonii) and Their Blood-Sucking Ectoparasites in Hokkaido, Japan

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Abstract

We investigated the prevalence of Bartonella in 123 northern bats (Eptesicus nilssonii) and their ectoparasites from Hokkaido, Japan. A total of 174 bat fleas (Ischnopsyllus needhami) and two bat bugs (Cimex japonicus) were collected from the bats. Bartonella bacteria were isolated from 32 (26.0%) of 123 bats. Though Bartonella DNA was detected in 79 (45.4%) of the bat fleas, the bacterium was isolated from only one bat flea (0.6%). The gltA sequences of the isolates were categorized into genotypes I, II, and III, which were found in both bats and their fleas. The gltA sequences of genotypes I and II showed 97.6% similarity with Bartonella strains from a Finnish E. nilssonii and a bat flea from a E. serotinus in the Netherlands. The rpoB sequences of the genotypes showed 98.9% similarity with Bartonella strain 44722 from E. serotinus in Republic of Georgia. The gltA and rpoB sequences of genotype III showed 95.9% and 96.7% similarity with Bartonella strains detected in shrews in Kenya and France, respectively. Phylogenetic analysis revealed that Bartonella isolates of genotypes I and II clustered with Bartonella strains from Eptesicus bats in Republic of Georgia and Finland, Myotis bats in Romania and the UK, and a bat flea from an Eptesicus bat in Finland. In contrast, genotype III formed a clade with B. florencae, B. acomydis, and B. birtlesii. These data suggest that northern bats in Japan harbor two Bartonella species and the bat flea serves as a potential vector of Bartonella transmission among the bats.

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References

  1. IUCN (2020) The IUCN Red List of Threatened Species. Version 2020–3. https://www.iucnredlist.org. Accessed 1 Mar 2021

  2. Simmons NB, Cirranello AL. 2020. Bat Species of the World: A taxonomic and geographic database. https://batnames.org/ Accessed 9 Au 2021

  3. Matsue M, Fujiwara N, Oshio T, et al (2006) A draft of the guideline for ecological surveys on bat species (in Japanese). http://www.nilim.go.jp/lab/bcg/siryou/tnn/tnn0354.htm. Accessed 1 Mar 2021

  4. Mühldorfer K (2013) Bats and bacterial pathogens: a review. Zoonoses Public Health 60:93–103. https://doi.org/10.1111/j.1863-2378.2012.01536.x

    Article  Google Scholar 

  5. Stuckey MJ, Chomel BB, de Fleurieu EC et al (2017) Bartonella, bats and bugs: a review. Comp Immunol Microbiol Infect Dis 55:20–29. https://doi.org/10.1016/j.cimid.2017.09.001

    Article  Google Scholar 

  6. Lin EY, Tsigrelis C, Baddour LM et al (2010) Candidatus Bartonella mayotimonensis and endocarditis. Emerg Infect Dis 16:500–503. https://doi.org/10.3201/eid1603.081673

    Article  CAS  Google Scholar 

  7. Veikkolainen V, Vesterinen EJ, Lilley TM, Pulliainen AT (2014) Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerg Infect Dis 20:960–967. https://doi.org/10.3201/eid2006.130956

    Article  Google Scholar 

  8. Stuckey MJ, Boulouis HJ, Cliquet F et al (2017) Potentially zoonotic bartonella in bats from France and Spain. Emerg Infect Dis 23:539–541. https://doi.org/10.3201/eid2303.160934

    Article  Google Scholar 

  9. Urushadze L, Bai Y, Osikowicz L et al (2017) Prevalence, diversity, and host associations of Bartonella strains in bats from Georgia (Caucasus). PLoS Negl Trop Dis 11:e0005428. https://doi.org/10.1371/journal.pntd.0005428

    Article  Google Scholar 

  10. Podsiadły E, Chmielewski T, Karbowiak G et al (2011) The occurrence of spotted fever rickettsioses and other tick-borne infections in forest workers in Poland. Vector-Borne Zoonotic Dis 11:985–989. https://doi.org/10.1089/vbz.2010.0080

    Article  Google Scholar 

  11. Chomel BB, Kasten RW, Floyd-Hawkins K et al (1996) Experimental transmission of Bartonella henselae by the cat flea. J Clin Microbiol 34:1952–1956. https://doi.org/10.1128/JCM.34.8.1952-1956.1996

    Article  CAS  Google Scholar 

  12. Bonilla DL, Kabeya H, Henn J et al (2009) Bartonella quintana in body lice and head lice from homeless persons, San Francisco, California, USA. Emerg Infect Dis 15:912–915. https://doi.org/10.3201/eid1506.090054

    Article  Google Scholar 

  13. Garcia-Quintanilla M, Dichter AA, Guerra H, Kempf VAJ (2019) Carrion’s disease: more than a neglected disease. Parasites Vectors 12:141. https://doi.org/10.1186/s13071-019-3390-2

    Article  Google Scholar 

  14. Sato S, Kabeya H, Ishiguro S et al (2021) Lipoptena fortisetosa as a vector of Bartonella bacteria in Japanese sika deer (Cervus nippon). Parasites Vectors 14:73. https://doi.org/10.1186/s13071-021-04585-w

    Article  CAS  Google Scholar 

  15. Nabeshima K, Sato S, Kabeya H et al (2020) Detection and phylogenetic analysis of Bartonella species from bat flies on eastern bent-wing bats (Miniopterus fuliginosus ) in Japan. Comp Immunol Microbiol Infect Dis 73:101570. https://doi.org/10.1016/j.cimid.2020.101570

    Article  Google Scholar 

  16. Reeves WK, Loftis AD, Gore JA, Dasch GA (2005) Molecular evidence for novel Bartonella species in Trichobius major (Diptera: Streblidae) and Cimex adjunctus (Hemiptera: Cimicidae) from two southeastern bat caves, U.S.A. J Vector Ecol 30:339–341

    Google Scholar 

  17. Judson SD, Frank HK, Hadly EA (2013) Bartonellae are prevalent and diverse in Costa Rican bats and bat flies. Zoonoses Public Health 62:609–617. https://doi.org/10.1111/zph.12188

    Article  CAS  Google Scholar 

  18. Brook CE, Bai Y, Dobson AP et al (2015) Bartonella spp. in fruit bats and blood-feeding ectoparasites in Madagascar. PLoS Negl Trop Dis 9:e0003532. https://doi.org/10.1371/journal.pntd.0003532

    Article  CAS  Google Scholar 

  19. Dietrich M, Tjale MA, Weyer J et al (2016) Diversity of Bartonella and Rickettsia spp. in bats and their blood-feeding ectoparasites from South Africa and Swaziland. PLoS One 11:e0152077. https://doi.org/10.1371/journal.pone.0152077

    Article  CAS  Google Scholar 

  20. Kamani J, Baneth G, Mitchell M et al (2014) Bartonella species in bats (Chiroptera) and bat flies (Nycteribiidae) from Nigeria, West Africa. Vector-Borne Zoonotic Dis 14:625–632. https://doi.org/10.1089/vbz.2013.1541

    Article  Google Scholar 

  21. Billeter SA, Hayman DTSS, Peel AJ et al (2012) Bartonella species in bat flies (Diptera: Nycteribiidae) from western Africa. Parasitology 139:324–329. https://doi.org/10.1017/S0031182011002113

    Article  CAS  Google Scholar 

  22. Morse SF, Olival KJ, Kosoy M et al (2012) Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae). Infect Genet Evol 12:1717–1723. https://doi.org/10.1016/j.meegid.2012.06.009

    Article  Google Scholar 

  23. Nabeshima K, Sato S, Kabeya H et al (2020) Isolation and genetic properties of Bartonella in eastern bent-wing bats (Miniopterus fuliginosus) in Japan. Infect Genet Evol 83:104354. https://doi.org/10.1016/j.meegid.2020.104354

    Article  CAS  Google Scholar 

  24. McKee CD, Kosoy MY, Bai Y et al (2017) Diversity and phylogenetic relationships among Bartonella strains from Thai bats. PLoS ONE 12:e0181696. https://doi.org/10.1371/journal.pone.0181696

    Article  CAS  Google Scholar 

  25. Anh PH, Van Cuong N, Son NT et al (2015) Diversity of Bartonella spp. in bats, southern Vietnam. Emerg Infect Dis 21:1266–1267. https://doi.org/10.3201/eid2107.141760

    Article  CAS  Google Scholar 

  26. Lin J-WW, Hsu Y-MM, Chomel BB et al (2012) Identification of novel Bartonella spp. in bats and evidence of Asian gray shrew as a new potential reservoir of Bartonella. Vet Microbiol 156:119–126. https://doi.org/10.1016/j.vetmic.2011.09.031

    Article  Google Scholar 

  27. Han H-JJ, Wen HL, Zhao L et al (2017) Novel Bartonella species in insectivorous bats, northern China. PLoS ONE 12:e0167915. https://doi.org/10.1371/journal.pone.0167915

    Article  CAS  Google Scholar 

  28. Sakaguti K (1962) Pacific Insects Monograph. Bernice P. Bishop Mus, Honolulu.

  29. Usinger R (1966) Monograph of Cimicidae (Hemiptera - Heteroptera). Entomological Society of America, College Park

    Google Scholar 

  30. Diaz MH, Bai Y, Malania L et al (2012) Development of a novel genus-specific real-time PCR assay for detection and differentiation of Bartonella species and genotypes. J Clin Microbiol 50:1645–1649. https://doi.org/10.1128/JCM.06621-11

    Article  CAS  Google Scholar 

  31. Norman AF, Regnery R, Jameson P et al (1995) Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol 33:1797–1803. https://doi.org/10.1128/JCM.33.7.1797-1803.1995

    Article  CAS  Google Scholar 

  32. Renesto P, Gouvernet J, Drancourt M et al (2001) Use of rpoB gene analysis for detection and identification of Bartonella species. J Clin Microbiol 39:430–437. https://doi.org/10.1128/JCM.39.2.430-437.2001

    Article  CAS  Google Scholar 

  33. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  Google Scholar 

  34. Burnham KP, Anderson DR (2004) Multimodel Inference: understanding AIC and BIC in Model Selection. Sociol Methods Res 33:261–304. https://doi.org/10.1177/0049124104268644

    Article  Google Scholar 

  35. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  36. McKee CD, Krawczyk AI, Sándor AD et al (2019) Host phylogeny, geographic overlap, and roost sharing shape parasite communities in European bats. Front Ecol Evol 7:69. https://doi.org/10.3389/fevo.2019.00069

    Article  Google Scholar 

  37. Halliday JEB, Knobel DL, Agwanda B, Bai Y, Breiman RF et al (2015) Prevalence and diversity of small mammal-associated Bartonella species in rural and urban Kenya. PLoS Negl Trop Dis 9:e0003608. https://doi.org/10.1371/journal.pntd.0003608

    Article  CAS  Google Scholar 

  38. Mediannikov O, El Karkouri K, Robert C et al (2013) Non-contiguous finished genome sequence and description of Bartonella florenciae sp. nov. Stand Genom Sci 9:185–196. https://doi.org/10.4056/sigs.4358060

    Article  CAS  Google Scholar 

  39. Concannon R, Wynn-Owen K, Simpson V, Birtles R (2005) Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology 131:489–496. https://doi.org/10.1017/S0031182005008097

    Article  CAS  Google Scholar 

  40. Corduneanu A, Sándor AD, Ionică AM et al (2018) Bartonella DNA in heart tissues of bats in central and eastern Europe and a review of phylogenetic relations of bat-associated bartonellae. Parasites Vectors 11:489. https://doi.org/10.1186/s13071-018-3070-7

    Article  CAS  Google Scholar 

  41. Inoue K, Maruyama S, Kabeya H et al (2009) Exotic small mammals as potential reservoirs of zoonotic Bartonella spp. Emerg Infect Dis 15:526–532. https://doi.org/10.3201/eid1504.081223

    Article  CAS  Google Scholar 

  42. Bermond D, Heller R, Barrat F et al (2000) Bartonella birtlesii sp. nov., isolated from small mammals (Apodemus spp.). Int J Syst Evol Microbiol 6:1973–1979. https://doi.org/10.1099/00207713-50-6-1973

    Article  Google Scholar 

  43. Orlova MV (2011) Ectoparasite associations of bats from Urals (Russia). Hystrix It J Mamm. 22. https://doi.org/10.4404/hystrix-22.1-4470

  44. Pearce RD, O’Shea TJ (2007) Ectoparasites in an urban population of big brown bats (Eptesicus fuscus) in Colorado. J Parasitol 93:518–530. https://doi.org/10.1645/GE-973R.1

    Article  Google Scholar 

  45. Szentiványi T, Estók P, Földvári M (2016) Checklist of host associations of European bat flies (Diptera: Nycteribiidae, Streblidae). Zootaxa 4205:zootaxa.4205.2.1. https://doi.org/10.11646/zootaxa.4205.2.1

  46. Dehio C, Sauder U, Hiestand R (2004) Isolation of Bartonella schoenbuchensis from Lipoptena cervi, a Blood-Sucking Arthropod Causing Deer Ked Dermatitis. J Clin Microbiol 42:5320–5323. https://doi.org/10.1128/JCM.42.11.5320-5323.2004

    Article  Google Scholar 

  47. Becker DJ, Bergner LM, Bentz AB et al (2018) Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats. PLoS Negl Trop Dis 12:e0006786. https://doi.org/10.1371/journal.pntd.0006786

    Article  Google Scholar 

  48. Frank HK, Boyd SD, Hadly EA (2018) Global fingerprint of humans on the distribution of Bartonella bacteria in mammals. PLoS Negl Trop Dis 12:e0006865. https://doi.org/10.1371/journal.pntd.0006865

    Article  Google Scholar 

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Acknowledgements

We want to thank Dr. Yuki Kobayashi, Nihon University for her assistance with bat sampling and suggestion for phylogenetic analysis of bat isolates.

Funding

This work was supported by the Grant-in Aid for Scientific Research from the Japan Society for the Promotion of Science [Grant number 18K06003].

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Authors and Affiliations

  1. Laboratory of Veterinary Public Health, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866, Kameino, Fujisawa, Kanagawa, 252-0880, Japan

    Kei Nabeshima, Shingo Sato, Murasaki Amano & Soichi Maruyama

  2. Ecological Risk Assessment and Control Section Center for Environmental Biology and Ecosystem, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki, 305-8506, Japan

    Kei Nabeshima

  3. Department of Biology, University of Richmond, 28 Westhampton Way, Richmond, VA, 23173, USA

    R. Jory Brinkerhoff

  4. Laboratory of Veterinary Food Hygiene, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866, Kameino, Fujisawa, Kanagawa, 252-0880, Japan

    Hidenori Kabeya

  5. Veterinary Research Center, College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa, 252-0880, Japan

    Takuya Itou

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  1. Kei Nabeshima
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  2. Shingo Sato
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Contributions

Kei Nabeshima: writing—original draft, methodology, investigation; Shingo Sato: methodology, investigation, writing—review and editing; Murasaki Amano: investigation; Jory R. Brinkerhoff: methodology, investigation, writing—review and editing; Hidenori Kabeya: writing—review and editing; Itou Takuya: investigation; Soichi Maruyama: resources, conceptualization, supervision, writing—review and editing.

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Correspondence to Soichi Maruyama.

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Nabeshima, K., Sato, S., Brinkerhoff, R.J. et al. Prevalence and Genetic Diversity of Bartonella Spp. in Northern Bats (Eptesicus nilssonii) and Their Blood-Sucking Ectoparasites in Hokkaido, Japan. Microb Ecol 85, 298–306 (2023). https://doi.org/10.1007/s00248-021-01935-0

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