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Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential

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 is...

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Autores principales: 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.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2928729/
https://www.ncbi.nlm.nih.gov/pubmed/20865041
http://dx.doi.org/10.1371/journal.pone.0012411
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author 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.
author_facet 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.
author_sort Yeoman, Carl J.
collection PubMed
description 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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spelling pubmed-29287292010-09-23 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. PLoS One Research Article 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. Public Library of Science 2010-08-26 /pmc/articles/PMC2928729/ /pubmed/20865041 http://dx.doi.org/10.1371/journal.pone.0012411 Text en Yeoman et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
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
title Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential
title_full Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential
title_fullStr Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential
title_full_unstemmed Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential
title_short Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential
title_sort comparative genomics of gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2928729/
https://www.ncbi.nlm.nih.gov/pubmed/20865041
http://dx.doi.org/10.1371/journal.pone.0012411
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