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

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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.

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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).

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Authors and Affiliations

  1. Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania

    Attila D. Sándor & Alexandra Corduneanu

  2. Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary

    Mihály Földvári & Dávid Kováts

  3. Natural History Museum, University of Oslo, Oslo, Norway

    Mihály Földvári

  4. Centre for Zoonoses & Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, the Netherlands

    Aleksandra I. Krawczyk & Hein Sprong

  5. Romanian Bat Protection Association – Central Branch, Odorheiu Secuiesc, Romania

    Levente Barti

  6. Department of Zoology, Hungarian Natural History Museum, Budapest, Hungary

    Tamás Görföl

  7. Department of Zoology, Eszterházy Károly University, Eger, Hungary

    Péter Estók

  8. Department of Parasitology and Zoology, University of Veterinary Medicine, 2 István Street, Budapest, H-1078, Hungary

    Sándor Szekeres, Sándor Hornok & Gábor Földvári

  9. Hungarian Department of Biology and Ecology, Babeş-Bolyai University, Cluj-Napoca, Romania

    Zoltán László

  10. Evolutionary Systems Research Group, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany, Hungary

    Gábor Földvári

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  1. Attila D. Sándor
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  2. Mihály Földvári
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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.

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Correspondence to Gábor Földvári.

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Electronic supplementary material

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)

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)

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Sándor, A.D., Földvári, M., Krawczyk, A.I. et al. Eco-epidemiology of Novel Bartonella Genotypes from Parasitic Flies of Insectivorous Bats. Microb Ecol 76, 1076–1088 (2018). https://doi.org/10.1007/s00248-018-1195-z

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