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Genetic diversity of Bartonella genotypes found in the striped field mouse (Apodemus agrarius) in Central Europe

Published online by Cambridge University Press:  09 June 2016

JASNA KRALJIK ,
ANNA PAZIEWSKA-HARRIS ,
DANA MIKLISOVÁ ,
LUCIA BLAŇAROVÁ ,
LADISLAV MOŠANSKÝ ,
MARTIN BONA  and
MICHAL STANKO
JASNA KRALJIK*
Affiliation:
Department of Vector-Borne Diseases, Institute of Parasitology SAS, Hlinkova 3, 040 01 Košice, Slovakia Department of Zoology, Faculty of Natural Sciences, Comenius University, 842 15 Bratislava 4, Mlynská dolina, Slovakia
ANNA PAZIEWSKA-HARRIS
Affiliation:
Parasitology Unit, Royal Tropical Institute, KIT Biomedical Research, Meibergdreef 39, 1105 AZ Amsterdam, The Netherlands
DANA MIKLISOVÁ
Affiliation:
Department of Vector-Borne Diseases, Institute of Parasitology SAS, Hlinkova 3, 040 01 Košice, Slovakia
LUCIA BLAŇAROVÁ
Affiliation:
Department of Vector-Borne Diseases, Institute of Parasitology SAS, Hlinkova 3, 040 01 Košice, Slovakia
LADISLAV MOŠANSKÝ
Affiliation:
Department of Vector-Borne Diseases, Institute of Parasitology SAS, Hlinkova 3, 040 01 Košice, Slovakia
MARTIN BONA
Affiliation:
Department of Anatomy, Faculty of Medicine, Pavol Jozef Šafárik University, Šrobárova 2, 041 80 Košice, Slovakia
MICHAL STANKO
Affiliation:
Department of Vector-Borne Diseases, Institute of Parasitology SAS, Hlinkova 3, 040 01 Košice, Slovakia
*
*Corresponding author: Department of Vector-Borne Diseases, Institute of Parasitology SAS, Hlinkova 3, 040 01 Košice, Slovakia. E-mail: kraljik@saske.sk
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Summary

We investigated the diversity of Bartonella in Apodemus agrarius, an important rodent of peri-domestic habitats, which has spread into Europe in the past 1000 years. Spleen samples of 344 A. agrarius from Eastern Slovakia were screened for the presence of Bartonella spp. using 16S–23S rRNA internal transcribed spacer region and bacteria were detected in 9% of rodents. Based on sequencing of three housekeeping genes (gltA, rpoB and groEL) Bartonella genotypes were ascribed to the species typical for mice and voles: B. grahamii, B. taylorii and B. birtlesii. However, the study also confirmed presence of genotypes belonging to the B. clarridgeiae/B. rochalimae clade, and the B. elizabethae/B. tribocorum clade, which are not commonly found in woodland rodents. In addition, a potential recombination event between these two genotypes was noted, which highlights an important role of A. agrarius in shaping Bartonella diversity and evolution.

Keywords

Bartonelladiversitystriped field mouseApodemus agrariusSlovakia
Type
Research Article
Information
Parasitology , Volume 143 , Issue 11 , September 2016 , pp. 1437 - 1442
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Berglund, E. C., Ellegaard, K., Granberg, F., Xie, Z., Maruyama, S., Kosoy, M. Y., Birtles, R. J. and Andersson, S. G. (2010). Rapid diversification by recombination in Bartonella grahamii from wild rodents in Asia contrasts with low levels of genomic divergence in Northern Europe and America. Molecular Ecology 19, 2241–2255.CrossRefGoogle ScholarPubMed
Bray, D. P., Bown, K. J., Stockley, P., Hurst, J. L., Bennett, M. and Birtles, R. J. (2007). Haemoparasites of common shrews (Sorex araneus) in Northwest England. Parasitology 134, 819–826.CrossRefGoogle ScholarPubMed
Buffet, J. P., Kosoy, M. and Vayssier-Taussat, M. (2013 a). Natural history of Bartonella infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiology 8, 1117–1128.CrossRefGoogle ScholarPubMed
Buffet, J. P., Pisanu, B., Brisse, S., Roussel, S., Felix, B., Halos, L., Chapuis, J. L. and Vayssier-Taussat, M. (2013 b). Deciphering Bartonella diversity, recombination, and host specificity in a rodent community. PLoS ONE 8, e68956.CrossRefGoogle Scholar
Deng, H., Le Rhun, D., Buffet, J. P., Cotte, V., Read, A., Birtles, R. J. and Vayssier-Taussat, M. (2012). Strategies of exploitation of mammalian reservoirs by Bartonella species. Veterinary Research 43, 15.CrossRefGoogle ScholarPubMed
Gundi, V. A., Billeter, S. A., Rood, M. P. and Kosoy, M. Y. (2012). Bartonella spp. in rats and zoonoses, Los Angeles, California, USA. Emerging Infectious Diseases 18, 631–633.CrossRefGoogle ScholarPubMed
Gutierrez, R., Krasnov, B., Morick, D., Gottlieb, Y., Khokhlova, I. S. and Harrus, S. (2015). Bartonella infection in rodents and their flea ectoparasites: an overview. Vector Borne and Zoonotic Diseases 15, 27–39.CrossRefGoogle ScholarPubMed
Guy, L., Nystedt, B., Toft, C., Zaremba-Niedzwiedzka, K., Berglund, E. C., Granberg, F., Naslund, K., Eriksson, A. S. and Andersson, S. G. (2013). A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella . PLoS Genetics 9, e1003393.CrossRefGoogle Scholar
Hildebrand, J., Paziewska-Harris, A., Zalesny, G. and Harris, P. D. (2013). PCR characterization suggests that an unusual range of Bartonella species infect the striped field mouse (Apodemus agrarius) in Central Europe. Applied and Environmental Microbiology 79, 5082–5084.CrossRefGoogle ScholarPubMed
Himsworth, C. G., Parsons, K. L., Jardine, C. and Patrick, D. M. (2013). Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne and Zoonotic Diseases 13, 349–359.CrossRefGoogle ScholarPubMed
Inoue, K., Maruyama, S., Kabeya, H., Hagiya, K., Izumi, Y., Une, Y. and Yoshikawa, Y. (2009). Exotic small mammals as potential reservoirs of zoonotic Bartonella spp. Emerging Infectious Diseases 15, 526–532.CrossRefGoogle ScholarPubMed
Knap, N., Duh, D., Birtles, R., Trilar, T., Petrovec, M. and Avsic-Zupanc, T. (2007). Molecular detection of Bartonella species infecting rodents in Slovenia. FEMS Immunology and Medical Microbiology 50, 45–50.CrossRefGoogle ScholarPubMed
Ko, S., Kang, J. G., Kim, H. C., Klein, T. A., Choi, K. S., Song, J. W., Youn, H. Y. and Chae, J. S. (2014). Prevalence, isolation and molecular characterization of Bartonella species in Republic of Korea. Transboundary and Emerging Diseases 63, 56–67.CrossRefGoogle ScholarPubMed
Kowalski, K. (2001). Pleistocene rodents of Europe. Folia Quaternaria 12, 3–389.Google Scholar
Lin, X. D., Wang, W., Guo, W. P., Zhang, X. H., Xing, J. G., Chen, S. Z., Li, M. H., Chen, Y., Xu, J., Plyusnin, A. and Zhang, Y. Z. (2012). Cross-species transmission in the speciation of the currently known murinae-associated hantaviruses. Journal of Virology 86, 11171–11182.CrossRefGoogle ScholarPubMed
Miller, M. A., Pfeiffer, W. and Schwartz, T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. In Gateway Computing Environments Workshop (GCE) pp. 1–8. IEEE, New Orleans, LA.Google Scholar
Paziewska, A., Harris, P. D., Zwolinska, L., Bajer, A. and Sinski, E. (2011). Recombination within and between species of the alpha proteobacterium Bartonella infecting rodents. Microbial Ecology 61, 134–145.CrossRefGoogle ScholarPubMed
Paziewska, A., Sinski, E. and Harris, P. D. (2012). Recombination, diversity and allele sharing of infectivity proteins between Bartonella species from rodents. Microbial Ecology 64, 525–536.CrossRefGoogle ScholarPubMed
Pelikán, J. (1965). Reproduction, population structure and elimination of males in Apodemus agrarius (Pall.). Zoologické listy 14, 317–332.Google Scholar
Rosický, B. (1957). Blechy – Aphaniptera . Fauna ČSR, ČSAV, Praha.Google Scholar
Sakka, H., Quéré, J. P., Kartavtseva, I., Pavlenko, M., Chelomina, G., Atopkin, D., Bogdanov, A. and Michaux, J. (2010). Comparative phylogeography of four Apodemus species (Mammalia: Rodentia) in the Asian Far East: evidence of Quaternary climatic changes in their genetic structure. Biological Journal of the Linnean Society of London 100, 797–821.CrossRefGoogle Scholar
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
StatSoft and Inc. (2013). STATISTICA (data analysis software system) 12·0.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Zalesny, G., Hildebrand, J., Paziewska-Harris, A., Behnke, J. M. and Harris, P. D. (2014). Heligmosomoides neopolygyrus Asakawa & Ohbayashi, 1986, a cryptic Asian nematode infecting the striped field mouse Apodemus agrarius in Central Europe. Parasites and Vectors 7, 457.CrossRefGoogle ScholarPubMed
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