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Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis

Porphyromonas gingivalis is a gram–negative anaerobic bacterium, a member of the human oral microbiome, and a proposed “keystone” pathogen in the development of chronic periodontitis, an inflammatory disease of the gingiva. P. gingivalis is a genetically diverse species, and is able to exchange chro...

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Autores principales: Kerr, Jennifer E., Abramian, Jared R., Dao, Doan-Hieu V., Rigney, Todd W., Fritz, Jamie, Pham, Tan, Gay, Isabel, Parthasarathy, Kavitha, Wang, Bing-yan, Zhang, Wenjian, Tribble, Gena D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3953592/
https://www.ncbi.nlm.nih.gov/pubmed/24626479
http://dx.doi.org/10.1371/journal.pone.0091696
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author Kerr, Jennifer E.
Abramian, Jared R.
Dao, Doan-Hieu V.
Rigney, Todd W.
Fritz, Jamie
Pham, Tan
Gay, Isabel
Parthasarathy, Kavitha
Wang, Bing-yan
Zhang, Wenjian
Tribble, Gena D.
author_facet Kerr, Jennifer E.
Abramian, Jared R.
Dao, Doan-Hieu V.
Rigney, Todd W.
Fritz, Jamie
Pham, Tan
Gay, Isabel
Parthasarathy, Kavitha
Wang, Bing-yan
Zhang, Wenjian
Tribble, Gena D.
author_sort Kerr, Jennifer E.
collection PubMed
description Porphyromonas gingivalis is a gram–negative anaerobic bacterium, a member of the human oral microbiome, and a proposed “keystone” pathogen in the development of chronic periodontitis, an inflammatory disease of the gingiva. P. gingivalis is a genetically diverse species, and is able to exchange chromosomal DNA between strains by natural competence and conjugation. In this study, we investigate the role of horizontal DNA transfer as an adaptive process to modify behavior, using the major fimbriae as our model system, due to their critical role in mediating interactions with the host environment. We show that P. gingivalis is able to exchange fimbrial allele types I and IV into four distinct strain backgrounds via natural competence. In all recombinants, we detected a complete exchange of the entire fimA allele, and the rate of exchange varies between the different strain backgrounds. In addition, gene exchange within other regions of the fimbrial genetic locus was identified. To measure the biological implications of these allele swaps we compared three genotypes of fimA in an isogenic background, strain ATCC 33277. We demonstrate that exchange of fimbrial allele type results in profound phenotypic changes, including the quantity of fimbriae elaborated, membrane blebbing, auto-aggregation and other virulence-associated phenotypes. Replacement of the type I allele with either the type III or IV allele resulted in increased invasion of gingival fibroblast cells relative to the isogenic parent strain. While genetic variability is known to impact host-microbiome interactions, this is the first study to quantitatively assess the adaptive effect of exchanging genes within the pan genome cloud. This is significant as it presents a potential mechanism by which opportunistic pathogens may acquire the traits necessary to modify host-microbial interactions.
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spelling pubmed-39535922014-03-18 Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis Kerr, Jennifer E. Abramian, Jared R. Dao, Doan-Hieu V. Rigney, Todd W. Fritz, Jamie Pham, Tan Gay, Isabel Parthasarathy, Kavitha Wang, Bing-yan Zhang, Wenjian Tribble, Gena D. PLoS One Research Article Porphyromonas gingivalis is a gram–negative anaerobic bacterium, a member of the human oral microbiome, and a proposed “keystone” pathogen in the development of chronic periodontitis, an inflammatory disease of the gingiva. P. gingivalis is a genetically diverse species, and is able to exchange chromosomal DNA between strains by natural competence and conjugation. In this study, we investigate the role of horizontal DNA transfer as an adaptive process to modify behavior, using the major fimbriae as our model system, due to their critical role in mediating interactions with the host environment. We show that P. gingivalis is able to exchange fimbrial allele types I and IV into four distinct strain backgrounds via natural competence. In all recombinants, we detected a complete exchange of the entire fimA allele, and the rate of exchange varies between the different strain backgrounds. In addition, gene exchange within other regions of the fimbrial genetic locus was identified. To measure the biological implications of these allele swaps we compared three genotypes of fimA in an isogenic background, strain ATCC 33277. We demonstrate that exchange of fimbrial allele type results in profound phenotypic changes, including the quantity of fimbriae elaborated, membrane blebbing, auto-aggregation and other virulence-associated phenotypes. Replacement of the type I allele with either the type III or IV allele resulted in increased invasion of gingival fibroblast cells relative to the isogenic parent strain. While genetic variability is known to impact host-microbiome interactions, this is the first study to quantitatively assess the adaptive effect of exchanging genes within the pan genome cloud. This is significant as it presents a potential mechanism by which opportunistic pathogens may acquire the traits necessary to modify host-microbial interactions. Public Library of Science 2014-03-13 /pmc/articles/PMC3953592/ /pubmed/24626479 http://dx.doi.org/10.1371/journal.pone.0091696 Text en © 2014 Kerr 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
Kerr, Jennifer E.
Abramian, Jared R.
Dao, Doan-Hieu V.
Rigney, Todd W.
Fritz, Jamie
Pham, Tan
Gay, Isabel
Parthasarathy, Kavitha
Wang, Bing-yan
Zhang, Wenjian
Tribble, Gena D.
Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis
title Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis
title_full Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis
title_fullStr Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis
title_full_unstemmed Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis
title_short Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis
title_sort genetic exchange of fimbrial alleles exemplifies the adaptive virulence strategy of porphyromonas gingivalis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3953592/
https://www.ncbi.nlm.nih.gov/pubmed/24626479
http://dx.doi.org/10.1371/journal.pone.0091696
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