1887

Abstract

Whole genome sequence analysis (digital DNA–DNA hybridization and average nucleotide identity) was carried out for 81 sequenced full genomes of the genus Gardnerella , including ten determined in this study, and indicated the existence of 13 genomic species, of which five consist of only one strain and of which only five contain more than four sequenced genomes. Furthermore, a collection of ten Gardnerella strains, representing the emended species G. vaginalis and the newly described species Gardnerella leopoldii, Gardnerella piotii and Gardnerella swidsinskii, was studied. Matrix-assisted laser desorption ionization time-of-flight MS analysis of the protein signatures identified specific peaks that can be used to differentiate these four species. Only strains of G. vaginalis produce β-galactosidase. We emend the description of G. vaginalis (type strain ATCC 14018=LMG 7832=CCUG 3717) and describe the novel species Gardnerella leopoldii sp. nov. (UGent 06.41=LMG 30814=CCUG 72425), Gardnerella piotii sp. nov. (UGent 18.01=LMG 30818=CCUG 72427) and Gardnerella swidsinskii sp. nov. (GS 9838-1=LMG 30812=CCUG 72429).

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2019-01-16
2024-12-02
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References

  1. Greenwood JR, Pickett MJ. Transfer of Haemophilus vaginalis Gardner and Dukes to a new genus, Gardnerella: G. vaginalis (Gardner and Dukes) comb. nov. Int J Syst Bacteriol 1980; 30:170–178 [View Article]
    [Google Scholar]
  2. Gardner HL, Dukes CD. New etiologic agent in nonspecific bacterial vaginitis. Science 1954; 120:853 [View Article][PubMed]
    [Google Scholar]
  3. Gardner HL, Dukes CD. Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis. Am J Obstet Gynecol 1955; 69:962–976[PubMed]
    [Google Scholar]
  4. Leopold S. Heretofore undescribed organism isolated from the genitourinary system. US Armed Forces Med J 1953; 4:263–266[PubMed]
    [Google Scholar]
  5. Piot P, van Dyck E, Peeters M, Hale J, Totten PA et al. Biotypes of Gardnerella vaginalis. J Clin Microbiol 1984; 20:677–679[PubMed]
    [Google Scholar]
  6. Ingianni A, Petruzzelli S, Morandotti G, Pompei R. Genotypic differentiation of Gardnerella vaginalis by amplified ribosomal DNA restriction analysis (ARDRA). FEMS Immunol Med Microbiol 1997; 18:61–66 [View Article][PubMed]
    [Google Scholar]
  7. Santiago GL, Deschaght P, El Aila N, Kiama TN, Verstraelen H et al. Gardnerella vaginalis comprises three distinct genotypes of which only two produce sialidase. Am J Obstet Gynecol 2011; 204:e1e7 [View Article][PubMed]
    [Google Scholar]
  8. Pleckaityte M, Janulaitiene M, Lasickiene R, Zvirbliene A. Genetic and biochemical diversity of Gardnerella vaginalis strains isolated from women with bacterial vaginosis. FEMS Immunol Med Microbiol 2012; 65:69–77 [View Article][PubMed]
    [Google Scholar]
  9. Schellenberg JJ, Paramel Jayaprakash T, Withana Gamage N, Patterson MH, Vaneechoutte M et al. Gardnerella vaginalis subgroups defined by cpn60 sequencing and sialidase activity in isolates from Canada, Belgium and Kenya. PLoS One 2016; 11:e0146510 [View Article][PubMed]
    [Google Scholar]
  10. Ahmed A, Earl J, Retchless A, Hillier SL, Rabe LK et al. Comparative genomic analyses of 17 clinical isolates of Gardnerella vaginalis provide evidence of multiple genetically isolated clades consistent with subspeciation into genovars. J Bacteriol 2012; 194:3922–3937 [View Article][PubMed]
    [Google Scholar]
  11. Balashov SV, Mordechai E, Adelson ME, Gygax SE. Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR. J Med Microbiol 2014; 63:162–175 [View Article][PubMed]
    [Google Scholar]
  12. Malki K, Shapiro JW, Price TK, Hilt EE, Thomas-White K et al. Genomes of Gardnerella strains reveal an abundance of prophages within the bladder microbiome. PLoS One 2016; 11:e0166757 [View Article][PubMed]
    [Google Scholar]
  13. Harwich MD, Alves JM, Buck GA, Strauss JF, Patterson JL et al. Drawing the line between commensal and pathogenic Gardnerella vaginalis through genome analysis and virulence studies. BMC Genomics 2010; 11:375 [View Article][PubMed]
    [Google Scholar]
  14. Janulaitiene M, Gegzna V, Baranauskiene L, Bulavaitė A, Simanavicius M et al. Phenotypic characterization of Gardnerella vaginalis subgroups suggests differences in their virulence potential. PLoS One 2018; 13:e0200625 [View Article][PubMed]
    [Google Scholar]
  15. Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article][PubMed]
    [Google Scholar]
  16. Yoon SH, Ha SM, 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]
  17. Cools P, Ho E, Vranckx K, Schelstraete P, Wurth B et al. Epidemic Achromobacter xylosoxidans strain among Belgian cystic fibrosis patients and review of literature. BMC Microbiol 2016; 16:122 [View Article][PubMed]
    [Google Scholar]
  18. Swidsinski A, Doerffel Y, Loening-Baucke V, Swidsinski S, Verstraelen H et al. Gardnerella biofilm involves females and males and is transmitted sexually. Gynecol Obstet Invest 2010; 70:256–263 [View Article][PubMed]
    [Google Scholar]
  19. El Aila NA, Tency I, Saerens B, de Backer E, Cools P et al. Strong correspondence in bacterial loads between the vagina and rectum of pregnant women. Res Microbiol 2011; 162:506–513 [View Article][PubMed]
    [Google Scholar]
  20. Catlin BW. Gardnerella vaginalis: characteristics, clinical considerations, and controversies. Clin Microbiol Rev 1992; 5:213–237 [View Article][PubMed]
    [Google Scholar]
  21. Turovskiy Y, Sutyak Noll K, Chikindas ML. The aetiology of bacterial vaginosis. J Appl Microbiol 2011; 110:1105–1128 [View Article][PubMed]
    [Google Scholar]
  22. Swidsinski A, Mendling W, Loening-Baucke V, Ladhoff A, Swidsinski S et al. Adherent biofilms in bacterial vaginosis. Obstet Gynecol 2005; 106:1013–1023 [View Article][PubMed]
    [Google Scholar]
  23. Janulaitiene M, Paliulyte V, Grinceviciene S, Zakareviciene J, Vladisauskiene A et al. Prevalence and distribution of Gardnerella vaginalis subgroups in women with and without bacterial vaginosis. BMC Infect Dis 2017; 17:394 [View Article][PubMed]
    [Google Scholar]
  24. Dunkelberg WE. Corynebacterium vaginale. Sex Transm Dis 1977; 4:69–75 [View Article][PubMed]
    [Google Scholar]
  25. Reyn A, Birch-Andersen A, Lapage SP. An electron microscope study of thin sections of Haemophilus vaginalis (Gardner and Dukes) and some possibly related species. Can J Microbiol 1966; 12:1125–1136 [View Article][PubMed]
    [Google Scholar]
  26. Sadhu K, Domingue PA, Chow AW, Nelligan J, Cheng N et al. Gardnerella vaginalis has a gram-positive cell-wall ultrastructure and lacks classical cell-wall lipopolysaccharide. J Med Microbiol 1989; 29:229–235 [View Article][PubMed]
    [Google Scholar]
  27. Harper JJ, Davis GHG. Cell wall analysis of Gardnerella vaginalis (Haemophilus vaginalis). Int J Syst Bacteriol 1982; 32:48–50 [View Article]
    [Google Scholar]
  28. O'Donnell AG, Minnikin DE, Goodfellow M, Piot P. Fatty acid, polar lipid and wall amino acid composition of Gardnerella vaginalis. Arch Microbiol 1984; 138:68–71 [View Article][PubMed]
    [Google Scholar]
  29. Mattarelli P, Holzapfel W, Franz CM, Endo A, Felis GE et al. Recommended minimal standards for description of new taxa of the genera Bifidobacterium, Lactobacillus and related genera. Int J Syst Evol Microbiol 2014; 64:1434–1451 [View Article][PubMed]
    [Google Scholar]
  30. van Esbroeck M, Vandamme P, Falsen E, Vancanneyt M, Moore E et al. Polyphasic approach to the classification and identification of Gardnerella vaginalis and unidentified Gardnerella vaginalis-like coryneforms present in bacterial vaginosis. Int J Syst Bacteriol 1996; 46:675–682 [View Article][PubMed]
    [Google Scholar]
  31. Yeoman CJ, Yildirim S, Thomas SM, Durkin AS, Torralba M et al. Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. PLoS One 2010; 5:e12411 [View Article][PubMed]
    [Google Scholar]
  32. Zhang G, Gao B, Adeolu M, Khadka B, Gupta RS. Phylogenomic analyses and comparative studies on genomes of the Bifidobacteriales: identification of molecular signatures specific for the order Bifidobacteriales and its different subclades. Front Microbiol 2016; 7:978 [View Article][PubMed]
    [Google Scholar]
  33. Lugli GA, Milani C, Turroni F, Duranti S, Mancabelli L et al. Comparative genomic and phylogenomic analyses of the Bifidobacteriaceae family. BMC Genomics 2017; 18:568 [View Article][PubMed]
    [Google Scholar]
  34. Gelber SE, Aguilar JL, Lewis KL, Ratner AJ. Functional and phylogenetic characterization of vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J Bacteriol 2008; 190:3896–3903 [View Article][PubMed]
    [Google Scholar]
  35. Hotze EM, Le HM, Sieber JR, Bruxvoort C, McInerney MJ et al. Identification and characterization of the first cholesterol-dependent cytolysins from Gram-negative bacteria. Infect Immun 2013; 81:216–225 [View Article][PubMed]
    [Google Scholar]
  36. Castro J, Alves P, Sousa C, Cereija T, França  et al. Using an in-vitro biofilm model to assess the virulence potential of bacterial vaginosis or non-bacterial vaginosis Gardnerella vaginalis isolates. Sci Rep 2015; 5:11640 [View Article][PubMed]
    [Google Scholar]
  37. Rampersaud R, Planet PJ, Randis TM, Kulkarni R, Aguilar JL et al. Inerolysin, a cholesterol-dependent cytolysin produced by Lactobacillus iners. J Bacteriol 2011; 193:1034–1041 [View Article][PubMed]
    [Google Scholar]
  38. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  39. Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K et al. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 2018; 68:2386–2392 [View Article][PubMed]
    [Google Scholar]
  40. Paramel Jayaprakash T, Schellenberg JJ, Hill JE. Resolution and characterization of distinct cpn60-based subgroups of Gardnerella vaginalis in the vaginal microbiota. PLoS One 2012; 7:e43009 [View Article][PubMed]
    [Google Scholar]
  41. Greenwood JR, Pickett MJ. Salient features of Haemophilus vaginalis. J Clin Microbiol 1979; 9:200–204[PubMed]
    [Google Scholar]
  42. Piot P, van Dyck E, Goodfellow M, Falkow S. A taxonomic study of Gardnerella vaginalis (Haemophilus vaginalis) Gardner and Dukes 1955. J Gen Microbiol 1980; 119:373–396 [View Article][PubMed]
    [Google Scholar]
  43. Piot P, van Dyck E, Totten PA, Holmes KK. Identification of Gardnerella (Haemophilus) vaginalis. J Clin Microbiol 1982; 15:19–24[PubMed]
    [Google Scholar]
  44. Taylor E, Phillips I. The identification of Gardnerella vaginalis. J Med Microbiol 1983; 16:83–92 [View Article][PubMed]
    [Google Scholar]
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