Two novel Bartonella (sub)species isolated from edible dormice (Glis glis): hints of cultivation stress-induced genomic changes

Oldřich Bartoš; Běla Klimešová; Karolina Volfová; Martin Chmel; Jiří Dresler; Petr Pajer; Hana Kabíčková; Peter Adamík; David Modrý; Alena Myslivcová Fučíková; Jan Votýpka

doi:10.3389/fmicb.2023.1289671

Two novel Bartonella (sub)species isolated from edible dormice (Glis glis): hints of cultivation stress-induced genomic changes

Front Microbiol. 2023 Nov 15:14:1289671. doi: 10.3389/fmicb.2023.1289671. eCollection 2023.

Authors

Oldřich Bartoš^#¹, Běla Klimešová^#², Karolina Volfová², Martin Chmel^{1

3}, Jiří Dresler¹, Petr Pajer¹, Hana Kabíčková¹, Peter Adamík^{4

5}, David Modrý^{6

7

8}, Alena Myslivcová Fučíková⁹, Jan Votýpka^{2

6}

Affiliations

¹ Military Health Institute, Military Medical Agency, Prague, Czechia.
² Department of Parasitology, Faculty of Science, Charles University, Prague, Czechia.
³ Department of Infectious Diseases, First Faculty of Medicine, Charles University and Military University Hospital Prague, Prague, Czechia.
⁴ Department of Zoology, Faculty of Science, Palacký University, Olomouc, Czechia.
⁵ Museum of Natural History, Olomouc, Czechia.
⁶ Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czechia.
⁷ Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czechia.
⁸ Department of Veterinary Sciences/CINeZ, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czechia.
⁹ Department of Biology, University of Hradec Králové, Hradec Králové, Czechia.

^# Contributed equally.

Abstract

Bartonelloses are neglected emerging infectious diseases caused by facultatively intracellular bacteria transmitted between vertebrate hosts by various arthropod vectors. The highest diversity of Bartonella species has been identified in rodents. Within this study we focused on the edible dormouse (Glis glis), a rodent with unique life-history traits that often enters households and whose possible role in the epidemiology of Bartonella infections had been previously unknown. We identified and cultivated two distinct Bartonella sub(species) significantly diverging from previously described species, which were characterized using growth characteristics, biochemical tests, and various molecular techniques including also proteomics. Two novel (sub)species were described: Bartonella grahamii subsp. shimonis subsp. nov. and Bartonella gliris sp. nov. We sequenced two individual strains per each described (sub)species. During exploratory genomic analyses comparing two genotypes ultimately belonging to the same species, both factually and most importantly even spatiotemporally, we noticed unexpectedly significant structural variation between them. We found that most of the detected structural variants could be explained either by prophage excision or integration. Based on a detailed study of one such event, we argue that prophage deletion represents the most probable explanation of the observed phenomena. Moreover, in one strain of Bartonella grahamii subsp. shimonis subsp. nov. we identified a deletion related to Bartonella Adhesin A, a major pathogenicity factor that modulates bacteria-host interactions. Altogether, our results suggest that even a limited number of passages induced sufficient selective pressure to promote significant changes at the level of the genome.

Keywords: Bartonella Adhesin A; Bartonella gliris; Bartonella grahamii subsp. shimonis; cultivation-related genomic changes; gene deletion.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by funding from projects of the Ministry of Interior, Czech Republic (VJ01010107: Extending and characterizing the collection of high-risk and risk biological causative agents of dangerous infectious diseases and implementing new procedures for working with them).