Skip to content
1887

Abstract

The genus comprises over 40 species, most of which are haemoparasites of mammals. Herein, we describe sp. nov., a novel member of the genus, isolated from field voles () in Kielder Forest, UK. Polyphasic characterization of three strains (C271, D105 and J117) of the proposed species indicated that they were closely related to members of phylogenetic lineage 3 (L3) of the genus. The average nucleotide identity (ANI) between C271 and other L3 species ranged between 88.8 and 90.6%, supporting the proposal of a new species. C271 shared ANIs approaching 96% with other members of L3 that are yet to be validly published but exhibited marked genomic, ecological and biogeographical differences from them, further justifying the creation of a new taxon. All three sp. nov. strains were found to possess genes encoding three VirB/D4 type IV secretion systems and associated effector proteins and to harbour a chromosomally integrated F-type conjugative plasmid, which forms an Hfr-like configuration not previously observed in the genus. This integration could facilitate large-scale chromosomal gene transfer during conjugation, with potential consequences for adaptation, recombination and niche differentiation. The phylogenetic structure of L3, coupled with the ecological partitioning of its members, suggests that covert host specificity, not generalism, is the dominant mode of diversification. The absence of the Trw system, which facilitates host switching in lineage 4 (L4), may constrain ecological breadth in L3, thought to be undergoing a parallel adaptive radiation with L4. The discovery of sp. nov. underscores the importance of combining genomic, ecological and evolutionary evidence when delimiting species boundaries in and raises new hypotheses about the role of Hfr-mediated recombination in the evolutionary dynamics of host-adapted pathogens. The type strain of sp. nov. is C271 (CSUR B1113, NCTC 15117).

Funding
This study was supported by the:
  • University of Salford Manchester
    • Principal Award Recipient: SeanPaul Brierley
  • Perry Foundation
    • Principal Award Recipient: SeanPaul Brierley
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.007095
2026-03-03
2026-03-17

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/ijsem/76/3/ijsem007095.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.007095&mimeType=html&fmt=ahah

References

  1. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  2. Neuvonen M-M, Tamarit D, Näslund K, Liebig J, Feldhaar H et al. The genome of Rhizobiales bacteria in predatory ants reveals urease gene functions but no genes for nitrogen fixation. Sci Rep 2016; 6:39197 [View Article] [PubMed]
    [Google Scholar]
  3. Bisch G, Neuvonen M-M, Pierce NE, Russell JA, Koga R et al. Genome evolution of Bartonellaceae symbionts of ants at the opposite ends of the trophic scale. Genome Biol Evol 2018; 10:1687–1704 [View Article] [PubMed]
    [Google Scholar]
  4. Kosoy M, Goodrich I. Comparative ecology of Bartonella and Brucella infections in wild carnivores. Front Vet Sci 2019; 5:322 [View Article]
    [Google Scholar]
  5. Buffet J-P, Pisanu B, Brisse S, Roussel S, Félix B et al. Deciphering Bartonella diversity, recombination, and host specificity in a rodent community. PLoS One 2013; 8:e68956 [View Article] [PubMed]
    [Google Scholar]
  6. Kosoy M, Hayman DTS, Chan KS. Bartonella bacteria in nature: where does population variability end and a species start?. Infect Genet Evol 2012; 12:894–904 [View Article]
    [Google Scholar]
  7. Kosoy M, Bai Y. Bartonella bacteria in urban rats: a movement from the jungles of Southeast Asia to metropoles around the globe. Front Ecol Evol 2019; 7:88 [View Article]
    [Google Scholar]
  8. Xu A, Lu L, Zhang W, Song X, Li G et al. Microevolution of Bartonella grahamii driven by geographic and host factors. mSystems 2024; 9:e0108924 [View Article] [PubMed]
    [Google Scholar]
  9. Maillard R, Riegel P, Barrat F, Bouillin C, Thibault D et al. Bartonella chomelii sp. nov., isolated from French domestic cattle (Bos taurus). Int J Syst Evol Microbiol 2004; 54:215–220 [View Article] [PubMed]
    [Google Scholar]
  10. Dehio C, Lanz C, Pohl R, Behrens P, Bermond D et al. Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. Int J Syst Evol Microbiol 2001; 51:1557–1565 [View Article] [PubMed]
    [Google Scholar]
  11. Wagner A, Dehio C. Role of distinct type-IV-secretion systems and secreted effector sets in host adaptation by pathogenic Bartonella species. Cell Microbiol 2019; 21:e13004 [View Article] [PubMed]
    [Google Scholar]
  12. Engel P, Salzburger W, Liesch M, Chang C-C, Maruyama S et al. Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella. PLoS Genet 2011; 7:e1001296 [View Article] [PubMed]
    [Google Scholar]
  13. Fromm K, Dehio C. The impact of Bartonella VirB/VirD4 type IV secretion system effectors on eukaryotic host cells. Front Microbiol 2021; 12:762582 [View Article] [PubMed]
    [Google Scholar]
  14. Harms A, Liesch M, Körner J, Québatte M, Engel P et al. A bacterial toxin-antitoxin module is the origin of inter-bacterial and inter-kingdom effectors of Bartonella. PLoS Genet 2017; 13:e1007077 [View Article] [PubMed]
    [Google Scholar]
  15. Deng HK, Le Rhun D, Le Naour E, Bonnet S, Vayssier-Taussat M. Identification of Bartonella Trw host-specific receptor on erythrocytes. PLoS One 2012; 7:e41447 [View Article] [PubMed]
    [Google Scholar]
  16. Chomel BB, Kasten RW. Bartonellosis, an increasingly recognized zoonosis. J Appl Microbiol 2010; 109:743–750 [View Article] [PubMed]
    [Google Scholar]
  17. Ernst E, Qurollo B, Olech C, Breitschwerdt EB. Bartonella rochalimae, a newly recognized pathogen in dogs. J Vet Intern Med 2020; 34:1447–1453 [View Article] [PubMed]
    [Google Scholar]
  18. Mendoza-Mujica G, Calvay-Sanchez KD, Zarate-Sulca Y, Jimenez-Vasquez V. New insights into the genomic information of an overlooked human pathogen: Bartonella rochalimae, causative agent of carrion’s disease. PLoS Negl Trop Dis 2025; 19:e0013040 [View Article] [PubMed]
    [Google Scholar]
  19. Bai Y, Gilbert A, Fox K, Osikowicz L, Kosoy M. Bartonella rochalimae and B. vinsonii subsp. berkhoffii in wild carnivores from Colorado, USA. J Wildl Dis 2016; 52:844–849 [View Article] [PubMed]
    [Google Scholar]
  20. Çelebi B, Zgheib R, Karataş A, Babür C, Öktem İMA et al. Bartonella species in small mammals in Turkey: Bartonella bilalgolemii sp. nov. isolated from a Ural field mouse (Apodemus uralensis). Vector Borne Zoonotic Dis 2025; 25:60–70 [View Article]
    [Google Scholar]
  21. Telfer S, Begon M, Bennett M, Bown KJ, Burthe S et al. Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology 2007; 134:413–425 [View Article] [PubMed]
    [Google Scholar]
  22. Withenshaw SM, Devevey G, Pedersen AB, Fenton A. Multihost Bartonella parasites display covert host specificity even when transmitted by generalist vectors. J Anim Ecol 2016; 85:1442–1452 [View Article] [PubMed]
    [Google Scholar]
  23. Tołkacz K, Alsarraf M, Kowalec M, Dwużnik D, Grzybek M et al. Bartonella infections in three species of Microtus: prevalence and genetic diversity, vertical transmission and the effect of concurrent Babesia microti infection on its success. Parasit Vectors 2018; 11:491 [View Article] [PubMed]
    [Google Scholar]
  24. Fischer ER, Hansen BT, Nair V, Hoyt FH, Schwartz CL et al. Scanning electron microscopy. Curr Protoc 2024; 4:e1034 [View Article] [PubMed]
    [Google Scholar]
  25. Chen S. Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp. Imeta 2023; 2:e107 [View Article] [PubMed]
    [Google Scholar]
  26. Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microbial Genomics 2017; 3:e000132 [View Article]
    [Google Scholar]
  27. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  28. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article] [PubMed]
    [Google Scholar]
  29. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
    [Google Scholar]
  30. Olson RD, Assaf R, Brettin T, Conrad N, Cucinell C et al. Introducing the bacterial and viral bioinformatics resource center (BV-BRC): a resource combining PATRIC, IRD and ViPR. Nucleic Acids Res 2023; 51:D678–D689 [View Article] [PubMed]
    [Google Scholar]
  31. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  32. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  33. Fournier PE, Couderc C, Buffet S, Flaudrops C, Raoult D. Rapid and cost-effective identification of Bartonella species using mass spectrometry. J Med Microbiol 2009; 58:1154–1159 [View Article] [PubMed]
    [Google Scholar]
  34. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  35. Québatte M, Dehio C. Bartonella gene transfer agent: Evolution, function, and proposed role in host adaptation. Cell Microbiol 2019; 21:e13068 [View Article] [PubMed]
    [Google Scholar]
  36. Gutiérrez R, Shalit T, Markus B, Yuan C, Nachum-Biala Y et al. Bartonella kosoyi sp. nov. and Bartonella krasnovii sp. nov., two novel species closely related to the zoonotic Bartonella elizabethae, isolated from black rats and wild desert rodent-fleas. Int J Syst Evol Microbiol 2020; 70:1656–1665 [View Article] [PubMed]
    [Google Scholar]
  37. Berglund EC, Frank AC, Calteau A, Vinnere Pettersson O, Granberg F et al. Run-off replication of host-adaptability genes is associated with gene transfer agents in the genome of mouse-infecting Bartonella grahamii. . PLoS Genet 2009; 5:e1000546 [View Article] [PubMed]
    [Google Scholar]
  38. Guy L, Nystedt B, Toft C, Zaremba-Niedzwiedzka K, Berglund EC et al. A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella. PLoS Genet 2013; 9:e1003393 [View Article] [PubMed]
    [Google Scholar]
  39. Lederberg J, Cavalli LL, Lederberg EM. Sex compatibility in Escherichia coli. Genetics 1952; 37:720–730 [View Article] [PubMed]
    [Google Scholar]
  40. Lawley TD, Klimke WA, Gubbins MJ, Frost LS. F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 2003; 224:1–15 [View Article] [PubMed]
    [Google Scholar]
  41. Koraimann G. Spread and persistence of virulence and antibiotic resistance genes: a ride on the F plasmid conjugation module. EcoSal Plus 2018; 8:10–128 [View Article] [PubMed]
    [Google Scholar]
  42. Sanchez-Nieves RL, Zhang C, Whitaker RJ. Integrated conjugative plasmid drives high frequency chromosomal gene transfer in Sulfolobus islandicus. Front Microbiol 2023; 14:1114574 [View Article] [PubMed]
    [Google Scholar]
  43. Derbyshire KM, Gray TA. Distributive conjugal transfer: new insights into horizontal gene transfer and genetic exchange in mycobacteria. Microbiol Spectr 2014; 2:MGM2–0022 [View Article] [PubMed]
    [Google Scholar]
  44. Silbert J, Lorenzo V de, Aparicio T. Refactoring the conjugation machinery of promiscuous plasmid RP4 into a device for conversion of gram-negative isolates to Hfr strains. ACS Synth Biol 2021; 10:690–697 [View Article] [PubMed]
    [Google Scholar]
  45. Young JPW, Moeskjær S, Afonin A, Rahi P, Maluk M et al. Defining the Rhizobium leguminosarum species complex. Genes 2021; 12:111 [View Article]
    [Google Scholar]
  46. Diop A, Torrance EL, Stott CM, Bobay LM. Gene flow and introgression are pervasive forces shaping the evolution of bacterial species. Genome Biol 2022; 23:239 [View Article] [PubMed]
    [Google Scholar]
  47. do Amaral RB, Cardozo MV, Varani A de M, Furquim MEC, Dias CM et al. First report of Bartonella spp. in marsupials from Brazil, with a description of Bartonella harrusi sp. nov. and a new proposal for the taxonomic reclassification of species of the genus Bartonella. Microorganisms 2022; 10:1609 [View Article] [PubMed]
    [Google Scholar]
  48. Buhler KJ, Fernando C, Hill JE, Galloway T, Carriere S et al. Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems. Parasit Vectors 2022; 15:366 [View Article] [PubMed]
    [Google Scholar]
  49. Rao H, Li S, Lu L, Wang R, Song X et al. Genetic diversity of Bartonella species in small mammals in the Qaidam Basin, Western China. Sci Rep 2021; 11:1735 [View Article] [PubMed]
    [Google Scholar]
  50. Birtles RJ, Hazel SM, Bennett M, Bown K, Raoult D et al. Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol Infect 2001; 126:323–329 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.007095
Loading
/content/journal/ijsem/10.1099/ijsem.0.007095
Loading

Data & Media loading...

Supplements

Supplementary material 1

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error