1887

Abstract

Members of the genus have been isolated from or detected in a wide range of animals, from non-human primates and felids to a rodent, the guinea pig. By means of selective culture, biochemical testing, Gram staining and PCR screening for the -specific internal transcribed spacer region of the rRNA operon, we isolated four strains of the genus from the oral cavity of the wild house mouse, subsp. The isolates are highly related and form a separate clade in the genus, as judged by tree analyses using either multi-locus sequence typing of ribosomal genes or core genes. One isolate, provisionally named sp. nov. (type strain AP2031=DSM 101846=CCUG 68283=LMG 29261), was studied further. Strain AP2031/ grew well . It was naturally competent, taking up DNA in a DNA uptake sequence and -dependent manner, and was amenable to genetic manipulation. These and other genomic attributes of sp. nov. make it an ideal candidate for use in developing a mouse model for studying –host interactions.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001237
2016-09-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/66/9/3585.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001237&mimeType=html&fmt=ahah

References

  1. Aas F. E., Egge-Jacobsen W., Winther-Larsen H. C., Løvold C., Hitchen P. G., Dell A., Koomey M. 2006; Neisseria gonorrhoeae type IV pili undergo multisite, hierarchical modifications with phosphoethanolamine and phosphocholine requiring an enzyme structurally related to lipopolysaccharide phosphoethanolamine transferases. J Biol Chem 281:27712–27723 [View Article][PubMed]
    [Google Scholar]
  2. Anonsen J. H., Egge-Jacobsen W., Aas F. E., Børud B., Koomey M., Vik A. 2012; Novel protein substrates of the phospho-form modification system in Neisseria gonorrhoeae and their connection to O-linked protein glycosylation. Infect Immun 80:22–30 [View Article][PubMed]
    [Google Scholar]
  3. Anonsen J. H., Vik Å., Borud B., Viburiene R., Aas F. E., Kidd S. W., Aspholm M., Koomey M. 2015; Characterizationof a unique tetrasaccharide and distinct glycoproteome in theO-linked protein glycosylation system of Neisseria elongata subspecies glycolytica . J Bacteriol 198:256–267 [View Article][PubMed]
    [Google Scholar]
  4. Barrett S. J., Sneath P. H. 1994; A numerical phenotypic taxonomic study of the genus Neisseria . Microbiology 140:2867–2891 [View Article][PubMed]
    [Google Scholar]
  5. Bennett J. S., Jolley K. A., Earle S. G., Corton C., Bentley S. D., Parkhill J., Maiden M. C. 2012; A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria . Microbiology 158:1570–1580 [View Article][PubMed]
    [Google Scholar]
  6. Bennett J. S., Jolley K. A., Maiden M. C. 2013; Genome sequence analyses show that Neisseria oralis is the same species as‘Neisseria mucosa var. heidelbergensis’ . Int J Syst Evol Microbiol 63:3920–3926 [View Article][PubMed]
    [Google Scholar]
  7. Bennett J. S., Bratcher H. B., Brehony C., Harrison O. B., Maiden M. C. 2014a; The Genus Neisseria . In The Prokaryotes – Alphaproteobacteria and Betaproteobacteria , pp. 881–900 Verlag: Springer; [CrossRef]
    [Google Scholar]
  8. Bennett J. S., Watkins E. R., Jolley K. A., Harrison O. B., Maiden M. C. 2014b; IdentifyingNeisseria species by use of the 50S ribosomal protein L6 (rplF) gene. J Clin Microbiol 52:1375–1381 [View Article]
    [Google Scholar]
  9. Berger U. 1960; Neisseria animalis nov. spec. Z Hyg Infektionskr 147:158–161 [View Article]
    [Google Scholar]
  10. Bhat K. S., Gibbs C. P., Barrera O., Morrison S. G., Jähnig F., Stern A., Kupsch E. M., Meyer T. F., Swanson J. 1991; The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol Microbiol 5:1889–1901 [View Article][PubMed]
    [Google Scholar]
  11. Bratcher H. B., Corton C., Jolley K. A., Parkhill J., Maiden M. C. 2014; A gene-by-gene population genomics platform: de novo assembly, annotation and genealogical analysis of 108 representative Neisseria meningitidis genomes. BMC Genomics 15:1138 [View Article][PubMed]
    [Google Scholar]
  12. Carbonnelle E., Helaine S., Nassif X., Pelicic V. 2006; A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol 61:1510–1522 [View Article][PubMed]
    [Google Scholar]
  13. Caugant D. A., Maiden M. C. 2009; Meningococcal carriage and disease–population biology and evolution. Vaccine 27:B64–B70 [View Article][PubMed]
    [Google Scholar]
  14. Cehovin A., Simpson P. J., McDowell M. A., Brown D. R., Noschese R., Pallett M., Brady J., Baldwin G. S., Lea S. M. et al. 2013; Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci USA 110:3065–3070 [View Article][PubMed]
    [Google Scholar]
  15. Chamot-Rooke J., Mikaty G., Malosse C., Soyer M., Dumont A., Gault J., Imhaus A. F., Martin P., Trellet M. et al. 2011; Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331:778–782 [View Article][PubMed]
    [Google Scholar]
  16. Cheesbrough M. 2006; Oxidase Test. In District Laboratory Practice in Tropical Countries Part 2 pp. 69–70 New York: Cambridge University Press; [CrossRef]
    [Google Scholar]
  17. Crooks G. E., Hon G., Chandonia J. M., Brenner S. E. 2004; WebLogo: a sequence logo generator. Genome Res 14:1188–1190 [View Article][PubMed]
    [Google Scholar]
  18. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  19. Dillard J. P. 2006; Genetic manipulation of Neisseria gonorrhoeae . In Current Protocols in Microbiology , pp. 4A.2.1–4A.2.19 Edited by Coico R., Kowalik T., Quarles J. M., Stevenson B., Taylor R. K., Simon A. E. New York: John Wiley and Sons;
    [Google Scholar]
  20. Eriksson J., Eriksson O. S., Jonsson A. B. 2012; Loss of meningococcal PilU delays microcolony formation and attenuates virulence in vivo . Infect Immun 80:2538–2547 [View Article][PubMed]
    [Google Scholar]
  21. Forest K. T., Dunham S. A., Koomey M., Tainer J. A. 1999; Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol 31:743–752 [View Article][PubMed]
    [Google Scholar]
  22. Frye S. A., Nilsen M., Tønjum T., Ambur O. H. 2013; Dialects of the DNA uptake sequence in Neisseriaceae . PLoS Genet 9:e1003458 [View Article][PubMed]
    [Google Scholar]
  23. Ganière J. P., Escande F., André-Fontaine G., Larrat M., Filloneau C. 1995; Characterization of group EF-4 bacteria from the oral cavity of dogs. Vet Microbiol 44:1–9 [View Article][PubMed]
    [Google Scholar]
  24. Giltner C. L., Nguyen Y., Burrows L. L. 2012; Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 76:740–772 [View Article][PubMed]
    [Google Scholar]
  25. Goris J., Konstantinidis K. T., Klappenbach J. A., Coenye T., Vandamme P., Tiedje J. M. 2007; DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91 [View Article][PubMed]
    [Google Scholar]
  26. Hall T. A. 1999; BioEdit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  27. Hamilton H. L., Dillard J. P. 2006; Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 59:376–385 [View Article][PubMed]
    [Google Scholar]
  28. Hartley M. D., Morrison M. J., Aas F. E., Børud B., Koomey M., Imperiali B. 2011; Biochemical characterization of the O-linked glycosylation pathway in Neisseria gonorrhoeae responsible for biosynthesis of protein glycans containing N,N'-diacetylbacillosamine. Biochemistry 50:4936–4948 [View Article][PubMed]
    [Google Scholar]
  29. Hélaine S., Carbonnelle E., Prouvensier L., Beretti J. L., Nassif X., Pelicic V. 2005; PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol Microbiol 55:65–77 [View Article][PubMed]
    [Google Scholar]
  30. Higashi D. L., Lee S. W., Snyder A., Weyand N. J., Bakke A., So M. 2007; Dynamics of Neisseria gonorrhoeae attachment: microcolony development, cortical plaque formation, and cytoprotection. Infect Immun 75:4743–4753 [View Article][PubMed]
    [Google Scholar]
  31. Higashi D. L., Biais N., Weyand N. J., Agellon A., Sisko J. L., Brown L. M., So M. 2011; N.elongata produces type IV pili that mediate interspecies gene transfer with N.gonorrhoeae . PLoS One 6:e21373 [View Article][PubMed]
    [Google Scholar]
  32. Howie H. L., Glogauer M., So M. 2005; TheN. gonorrhoeae type IV pilus stimulates mechanosensitive pathways and cytoprotection through a pilT-dependent mechanism. PLoS Biol 3:e100 [View Article][PubMed]
    [Google Scholar]
  33. Jennings M. P., Jen F. E., Roddam L. F., Apicella M. A., Edwards J. L. 2011; Neisseria gonorrhoeae pilin glycan contributes to CR3 activation during challenge of primary cervical epithelial cells. Cell Microbiol 13:885–896 [View Article][PubMed]
    [Google Scholar]
  34. Jolley K. A., Maiden M. C. 2010; BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595 [View Article][PubMed]
    [Google Scholar]
  35. Jolley K. A., Bliss C. M., Bennett J. S., Bratcher H. B., Brehony C., Colles F. M., Wimalarathna H., Harrison O. B., Sheppard S. K. et al. 2012; Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158:1005–1015 [View Article][PubMed]
    [Google Scholar]
  36. Kurre R., Höne A., Clausen M., Meel C., Maier B. 2012; PilT2 enhances the speed of gonococcal type IV pilus retraction and of twitching motility. Mol Microbiol 86:857–865 [View Article][PubMed]
    [Google Scholar]
  37. Lee S. W., Higashi D. L., Snyder A., Merz A. J., Potter L., So M. 2005; PilT is required for PI(3, 4, 5)P3-mediated crosstalk between Neisseria gonorrhoeae and epithelial cells. Cell Microbiol 7:1271–1284 [View Article][PubMed]
    [Google Scholar]
  38. Liu G., Tang C. M., Exley R. M. 2015; Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus. Microbiology 161:1297–1312 [View Article][PubMed]
    [Google Scholar]
  39. Long C. D., Madraswala R. N., Seifert H. S. 1998; Comparisons between colony phase variation of Neisseria gonorrhoeae FA1090 and pilus, pilin, and S-pilin expression. Infect Immun 66:1918–1927[PubMed]
    [Google Scholar]
  40. Marceau M., Forest K., Béretti J. L., Tainer J., Nassif X. 1998; Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol 27:705–715 [View Article][PubMed]
    [Google Scholar]
  41. Marri P. R., Paniscus M., Weyand N. J., Rendón M. A., Calton C. M., Hernández D. R., Higashi D. L., Sodergren E., Weinstock G. M. et al. 2010; Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 5:e11835 [View Article][PubMed]
    [Google Scholar]
  42. Mell J. C., Redfield R. J. 2014; Natural competence and the evolution of DNA uptake specificity. J Bacteriol 196:1471–1483 [View Article][PubMed]
    [Google Scholar]
  43. Merz A. J., Rifenbery D. B., Arvidson C. G., So M. 1996; Traversal of a polarized epithelium by pathogenic Neisseriae: facilitation by type IV pili and maintenance of epithelial barrier function. Mol Med 2:745–754[PubMed]
    [Google Scholar]
  44. Merz A. J., Enns C. A., So M. 1999; Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol Microbiol 32:1316–1332 [View Article][PubMed]
    [Google Scholar]
  45. Merz A. J., So M., Sheetz M. P. 2000; Pilus retraction powers bacterial twitching motility. Nature 407:98–102 [View Article][PubMed]
    [Google Scholar]
  46. Murphy J., Devane M. L., Robson B., Gilpin B. J. 2005; Genotypic characterization of bacteria cultured from duck faeces. J Appl Microbiol 99:301–309 [View Article][PubMed]
    [Google Scholar]
  47. Naessan C. L., Egge-Jacobsen W., Heiniger R. W., Wolfgang M. C., Aas F. E., Røhr A., Winther-Larsen H. C., Koomey M. 2008; Genetic and functional analyses of PptA, a phospho-form transferase targeting type IV pili in Neisseria gonorrhoeae . J Bacteriol 190:387–400 [View Article][PubMed]
    [Google Scholar]
  48. Nassif X., Beretti J. L., Lowy J., Stenberg P., O'Gaora P., Pfeifer J., Normark S., So M. 1994; Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci USA 91:3769–3773 [View Article][PubMed]
    [Google Scholar]
  49. Pujol C., Eugène E., Marceau M., Nassif X. 1999; The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc Natl Acad Sci USA 96:4017–4022 [View Article][PubMed]
    [Google Scholar]
  50. Read R. C. 2014; Neisseria meningitidis; clones, carriage, and disease. Clin Microbiol Infect 20:391–395 [View Article][PubMed]
    [Google Scholar]
  51. Rice P., Longden I., Bleasby A. 2000; EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277 [View Article][PubMed]
    [Google Scholar]
  52. Sneath P. H., Barrett S. J. 1996; A new species of Neisseria from the dental plaque of the domestic cow, Neisseria dentiae sp. nov. Lett Appl Microbiol 23:355–358 [View Article][PubMed]
    [Google Scholar]
  53. Swanson J., Kraus S. J., Gotschlich E. C. 1971; Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med 134:886–906[PubMed] [CrossRef]
    [Google Scholar]
  54. Swanson J., Barrera O. 1983; Gonococcal pilus subunit size heterogeneity correlates with transitions in colony piliation phenotype, not with changes in colony opacity. J Exp Med 158:1459–1472 [View Article][PubMed]
    [Google Scholar]
  55. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  56. Tonjum T. 2005; GenusI. Neisseria Trevisan 1885, 105AL. In Bergey's Manual of Systematic Bacteriology pp. 777–798 Edited by Brenner D. J., Krieg N. R., Staley J. T., Garrity G. M. New York: Springer; [CrossRef]
    [Google Scholar]
  57. Turner C. F., Rogers S. M., Miller H. G., Miller W. C., Gribble J. N., Chromy J. R., Leone P. A., Cooley P. C., Quinn T. C., Zenilman J. M. 2002; Untreated gonococcal and chlamydial infection in a probability sample of adults. JAMA 287:726–733 [View Article][PubMed]
    [Google Scholar]
  58. Veyrier F. J., Biais N., Morales P., Belkacem N., Guilhen C., Ranjeva S., Sismeiro O., Péhau-Arnaudet G., Rocha E. P. et al. 2015; Common cell shape evolution of two nasopharyngeal pathogens. PLoS Genet 11:e1005338 [View Article][PubMed]
    [Google Scholar]
  59. Walstad D. L., Guymon L. F., Sparling P. F. 1977; Altered outer membrane protein in different colonial types of Neisseria gonorrhoeae . J Bacteriol 129:1623–1627
    [Google Scholar]
  60. Weyand N. J., Wertheimer A. M., Hobbs T. R., Sisko J. L., Taku N. A., Gregston L. D., Clary S., Higashi D. L., Biais N. et al. 2013; Neisseria infection of rhesus macaques as a model to study colonization, transmission, persistence, and horizontal gene transfer. Proc Natl Acad Sci USA 110:3059–3064 [View Article]
    [Google Scholar]
  61. Winther-Larsen H. C., Hegge F. T., Wolfgang M., Hayes S. F., van Putten J. P., Koomey M. 2001; Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 98:15276–15281 [View Article][PubMed]
    [Google Scholar]
  62. Wolfgang M., Lauer P., Park H. S., Brossay L., Hébert J., Koomey M. 1998; PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae . Mol Microbiol 29:321–330 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.001237
Loading
/content/journal/ijsem/10.1099/ijsem.0.001237
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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