Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential

Carl J. Yeoman, Suleyman Yildirim, Susan M. Thomas, A. Scott Durkin, Manolito Torralba, Granger Sutton, Christian J. Buhay, Yan Ding, Shannon P. Dugan-Rocha, Donna M. Muzny, Xiang Qin, Richard A. Gibbs, Steven R. Leigh, Rebecca Stumpf, Bryan A. White, Sarah K. Highlander, Karen E. Nelson, Brenda A. Wilson

Research output: Contribution to journalArticle

Abstract

Background: Gardnerella vaginalis is described as a common vaginal bacterial species whose presence correlates strongly with bacterial vaginosis (BV). Here we report the genome sequencing and comparative analyses of three strains of G. vaginalis. Strains 317 (ATCC 14019) and 594 (ATCC 14018) were isolated from the vaginal tracts of women with symptomatic BV, while Strain 409-05 was isolated from a healthy, asymptomatic individual with a Nugent score of 9. Principal Findings: Substantial genomic rearrangement and heterogeneity were observed that appeared to have resulted from both mobile elements and substantial lateral gene transfer. These genomic differences translated to differences in metabolic potential. All strains are equipped with significant virulence potential, including genes encoding the previously described vaginolysin, pili for cytoadhesion, EPS biosynthetic genes for biofilm formation, and antimicrobial resistance systems, We also observed systems promoting multi-drug and lantibiotic extrusion. All G. vaginalis strains possess a large number of genes that may enhance their ability to compete with and exclude other vaginal colonists. These include up to six toxin-antitoxin systems and up to nine additional antitoxins lacking cognate toxins, several of which are clustered within each genome. All strains encode bacteriocidal toxins, including two lysozyme-like toxins produced uniquely by strain 409- 05. Interestingly, the BV isolates encode numerous proteins not found in strain 409-05 that likely increase their pathogenic potential. These include enzymes enabling mucin degradation, a trait previously described to strongly correlate with BV, although commonly attributed to non-G. vaginalis species. Conclusions: Collectively, our results indicate that all three strains are able to thrive in vaginal environments, and therein the BV isolates are capable of occupying a niche that is unique from 409-05. Each strain has significant virulence potential, although genomic and metabolic differences, such as the ability to degrade mucin, indicate that the detection of G. vaginalis in the vaginal tract provides only partial information on the physiological potential of the organism.

Original languageEnglish (US)
Article numbere12411
JournalPloS one
Volume5
Issue number8
DOIs
StatePublished - Oct 20 2010

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Gardnerella vaginalis
Bacterial Vaginosis
Genomics
Virulence
virulence
genomics
Antitoxins
Mucins
Genes
toxins
Genome
antitoxins
Horizontal Gene Transfer
Bacteriocins
mucins
Biofilms
Muramidase
Gene transfer
Gene encoding
genome

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. / Yeoman, Carl J.; Yildirim, Suleyman; Thomas, Susan M.; Durkin, A. Scott; Torralba, Manolito; Sutton, Granger; Buhay, Christian J.; Ding, Yan; Dugan-Rocha, Shannon P.; Muzny, Donna M.; Qin, Xiang; Gibbs, Richard A.; Leigh, Steven R.; Stumpf, Rebecca; White, Bryan A.; Highlander, Sarah K.; Nelson, Karen E.; Wilson, Brenda A.

In: PloS one, Vol. 5, No. 8, e12411, 20.10.2010.

Research output: Contribution to journalArticle

Yeoman, CJ, Yildirim, S, Thomas, SM, Durkin, AS, Torralba, M, Sutton, G, Buhay, CJ, Ding, Y, Dugan-Rocha, SP, Muzny, DM, Qin, X, Gibbs, RA, Leigh, SR, Stumpf, R, White, BA, Highlander, SK, Nelson, KE & Wilson, BA 2010, 'Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential', PloS one, vol. 5, no. 8, e12411. https://doi.org/10.1371/journal.pone.0012411
Yeoman, Carl J. ; Yildirim, Suleyman ; Thomas, Susan M. ; Durkin, A. Scott ; Torralba, Manolito ; Sutton, Granger ; Buhay, Christian J. ; Ding, Yan ; Dugan-Rocha, Shannon P. ; Muzny, Donna M. ; Qin, Xiang ; Gibbs, Richard A. ; Leigh, Steven R. ; Stumpf, Rebecca ; White, Bryan A. ; Highlander, Sarah K. ; Nelson, Karen E. ; Wilson, Brenda A. / Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. In: PloS one. 2010 ; Vol. 5, No. 8.
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abstract = "Background: Gardnerella vaginalis is described as a common vaginal bacterial species whose presence correlates strongly with bacterial vaginosis (BV). Here we report the genome sequencing and comparative analyses of three strains of G. vaginalis. Strains 317 (ATCC 14019) and 594 (ATCC 14018) were isolated from the vaginal tracts of women with symptomatic BV, while Strain 409-05 was isolated from a healthy, asymptomatic individual with a Nugent score of 9. Principal Findings: Substantial genomic rearrangement and heterogeneity were observed that appeared to have resulted from both mobile elements and substantial lateral gene transfer. These genomic differences translated to differences in metabolic potential. All strains are equipped with significant virulence potential, including genes encoding the previously described vaginolysin, pili for cytoadhesion, EPS biosynthetic genes for biofilm formation, and antimicrobial resistance systems, We also observed systems promoting multi-drug and lantibiotic extrusion. All G. vaginalis strains possess a large number of genes that may enhance their ability to compete with and exclude other vaginal colonists. These include up to six toxin-antitoxin systems and up to nine additional antitoxins lacking cognate toxins, several of which are clustered within each genome. All strains encode bacteriocidal toxins, including two lysozyme-like toxins produced uniquely by strain 409- 05. Interestingly, the BV isolates encode numerous proteins not found in strain 409-05 that likely increase their pathogenic potential. These include enzymes enabling mucin degradation, a trait previously described to strongly correlate with BV, although commonly attributed to non-G. vaginalis species. Conclusions: Collectively, our results indicate that all three strains are able to thrive in vaginal environments, and therein the BV isolates are capable of occupying a niche that is unique from 409-05. Each strain has significant virulence potential, although genomic and metabolic differences, such as the ability to degrade mucin, indicate that the detection of G. vaginalis in the vaginal tract provides only partial information on the physiological potential of the organism.",
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AU - Thomas, Susan M.

AU - Durkin, A. Scott

AU - Torralba, Manolito

AU - Sutton, Granger

AU - Buhay, Christian J.

AU - Ding, Yan

AU - Dugan-Rocha, Shannon P.

AU - Muzny, Donna M.

AU - Qin, Xiang

AU - Gibbs, Richard A.

AU - Leigh, Steven R.

AU - Stumpf, Rebecca

AU - White, Bryan A.

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