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Microbial Ecology

, Volume 76, Issue 4, pp 1076–1088 | Cite as

Eco-epidemiology of Novel Bartonella Genotypes from Parasitic Flies of Insectivorous Bats

  • Attila D. Sándor
  • Mihály Földvári
  • Aleksandra I. Krawczyk
  • Hein Sprong
  • Alexandra Corduneanu
  • Levente Barti
  • Tamás Görföl
  • Péter Estók
  • Dávid Kováts
  • Sándor Szekeres
  • Zoltán László
  • Sándor Hornok
  • Gábor FöldváriEmail author
Host Microbe Interactions

Abstract

Bats are important zoonotic reservoirs for many pathogens worldwide. Although their highly specialized ectoparasites, bat flies (Diptera: Hippoboscoidea), can transmit Bartonella bacteria including human pathogens, their eco-epidemiology is unexplored. Here, we analyzed the prevalence and diversity of Bartonella strains sampled from 10 bat fly species from 14 European bat species. We found high prevalence of Bartonella spp. in most bat fly species with wide geographical distribution. Bat species explained most of the variance in Bartonella distribution with the highest prevalence of infected flies recorded in species living in dense groups exclusively in caves. Bat gender but not bat fly gender was also an important factor with the more mobile male bats giving more opportunity for the ectoparasites to access several host individuals. We detected high diversity of Bartonella strains (18 sequences, 7 genotypes, in 9 bat fly species) comparable with tropical assemblages of bat-bat fly association. Most genotypes are novel (15 out of 18 recorded strains have a similarity of 92–99%, with three sequences having 100% similarity to Bartonella spp. sequences deposited in GenBank) with currently unknown pathogenicity; however, 4 of these sequences are similar (up to 92% sequence similarity) to Bartonella spp. with known zoonotic potential. The high prevalence and diversity of Bartonella spp. suggests a long shared evolution of these bacteria with bat flies and bats providing excellent study targets for the eco-epidemiology of host-vector-pathogen cycles.

Keywords

Chiroptera Bartonella Bat Fly Host-parasite Coevolution Nycteribiidae Pathogen Diversity 

Notes

Acknowledgements

Permission for bat capture was provided by the National Inspectorate for Environment, Nature and Water (Hungary), and the Underground Heritage Commission (Romania). Bat banding license numbers are 59/2003 (PE), 305/2015 (ADS), and TMF-493/3/2005 (TG). No live bat was harmed for this study. The authors thank C. Jére, I. Csősz, D. Bălășoiu, A. Telea, and A. Ionică for their contribution in the bat fly collection in Romania. We would like to express our thanks to Cristian Domșa for the help provided in the creation of the maps in Figs. 1 and 6. The survey was organized in the framework of the EurNegVec COST Action TD1303. This research was supported from the grant PN-II-RU-TE-2014-4-1389, the grant “In the light of evolution: theories and solutions” (GINOP-2.3.2-15-2016-00057), and the János Bolyai Research Scholarship of the Hungarian Academy of Science (to ADS and GF).

Authors’ Contributions

ADS initiated the study, did part of the sample collection, and wrote the manuscript. LB, AC, SH, TG, PE, ZL, and DK contributed important samples to the study. MF identified all bat flies. AK, SSz, and HS performed the molecular and phylogenetic analyses. GF organized part of the sample collection and contributed to the study design and manuscript preparation. All authors read and approved the final version of the manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1195_MOESM1_ESM.pdf (66 kb)
Figure S1 Neighbor-joining phylogenetic tree based on the multiple alignment of the gltaA gene, including Bartonella sequences obtained in this study. Clusters were assigned based on visual inspection of the tree. (PDF 65 kb)
248_2018_1195_MOESM2_ESM.pdf (31 kb)
Supplementary Figure S2 Neighbor-joining phylogenetic tree based on the pairwise alignment of an approx. 360 bp long fragment of the gltaA gene, including representative Bartonella sequences obtained in this study (highlighted by green fonts and 5 character codes) and representative sequences of other Bartonella spp. retrieved from GenBank. Sequences in blue represent Bartonella spp. related to bats or bat flies, while sequences in black denote Bartonella spp. from other host species, Bartonella spp. with known pathogenicity are highlighted in bold. (PDF 31 kb)
248_2018_1195_MOESM3_ESM.xlsx (11 kb)
Table S1 (XLSX 11 kb)
248_2018_1195_MOESM4_ESM.xlsx (36 kb)
Table S2 (XLSX 35 kb)
248_2018_1195_MOESM5_ESM.xlsx (11 kb)
Table S3 (XLSX 10 kb)
248_2018_1195_MOESM6_ESM.docx (15 kb)
Table S4 (DOCX 15 kb)
248_2018_1195_MOESM7_ESM.xlsx (11 kb)
Table S5 (XLSX 10 kb)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Attila D. Sándor
    • 1
  • Mihály Földvári
    • 2
    • 3
  • Aleksandra I. Krawczyk
    • 4
  • Hein Sprong
    • 4
  • Alexandra Corduneanu
    • 1
  • Levente Barti
    • 5
  • Tamás Görföl
    • 6
  • Péter Estók
    • 7
  • Dávid Kováts
    • 2
  • Sándor Szekeres
    • 8
  • Zoltán László
    • 9
  • Sándor Hornok
    • 8
  • Gábor Földvári
    • 8
    • 10
    Email author
  1. 1.Department of Parasitology and Parasitic DiseasesUniversity of Agricultural Sciences and Veterinary MedicineCluj-NapocaRomania
  2. 2.Department of Evolutionary Zoology and Human BiologyUniversity of DebrecenDebrecenHungary
  3. 3.Natural History MuseumUniversity of OsloOsloNorway
  4. 4.Centre for Zoonoses & Environmental Microbiology, Centre for Infectious Disease ControlNational Institute for Public Health and the EnvironmentBilthoventhe Netherlands
  5. 5.Romanian Bat Protection Association – Central BranchOdorheiu SecuiescRomania
  6. 6.Department of ZoologyHungarian Natural History MuseumBudapestHungary
  7. 7.Department of ZoologyEszterházy Károly UniversityEgerHungary
  8. 8.Department of Parasitology and ZoologyUniversity of Veterinary MedicineBudapestHungary
  9. 9.Hungarian Department of Biology and EcologyBabeş-Bolyai UniversityCluj-NapocaRomania
  10. 10.Evolutionary Systems Research Group, Centre for Ecological ResearchHungarian Academy of SciencesTihanyHungary

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