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Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq

Many bacterial infections involve polymicrobial communities in which constituent organisms are synergistically pathogenic. Periodontitis, a commonly occurring chronic inflammatory disorder, is induced by multispecies bacterial communities. The periodontal keystone pathogen Porphyromonas gingivalis a...

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Autores principales: Hendrickson, Erik L., Beck, David A. C., Miller, Daniel P., Wang, Qian, Whiteley, Marvin, Lamont, Richard J., Hackett, Murray
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5329018/
https://www.ncbi.nlm.nih.gov/pubmed/28293219
http://dx.doi.org/10.3389/fmicb.2017.00261
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author Hendrickson, Erik L.
Beck, David A. C.
Miller, Daniel P.
Wang, Qian
Whiteley, Marvin
Lamont, Richard J.
Hackett, Murray
author_facet Hendrickson, Erik L.
Beck, David A. C.
Miller, Daniel P.
Wang, Qian
Whiteley, Marvin
Lamont, Richard J.
Hackett, Murray
author_sort Hendrickson, Erik L.
collection PubMed
description Many bacterial infections involve polymicrobial communities in which constituent organisms are synergistically pathogenic. Periodontitis, a commonly occurring chronic inflammatory disorder, is induced by multispecies bacterial communities. The periodontal keystone pathogen Porphyromonas gingivalis and the accessory pathogen Streptococcus gordonii exhibit polymicrobial synergy in animal models of disease. Mechanisms of co-adhesion and community formation by P. gingivalis and S. gordonii are well-established; however, little is known regarding the basis for increased pathogenicity. In this study we used time-coursed RNA-Seq to comprehensively and quantitatively examine the dynamic transcriptional landscape of P. gingivalis in a model consortium with S. gordonii. Genes encoding a number of potential virulence determinants had higher relative mRNA levels in the context of dual species model communities than P. gingivalis alone, including adhesins, the Type IX secretion apparatus, and tetratricopeptide repeat (TPR) motif proteins. In contrast, genes encoding conjugation systems and many of the stress responses showed lower levels of expression in P. gingivalis. A notable exception to reduced abundance of stress response transcripts was the genes encoding components of the oxidative stress-related OxyR regulon, indicating an adaptation of P. gingivalis to detoxify peroxide produced by the streptococcus. Collectively, the results are consistent with evolutionary adaptation of P. gingivalis to a polymicrobial oral environment, one outcome of which is increased pathogenic potential.
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spelling pubmed-53290182017-03-14 Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq Hendrickson, Erik L. Beck, David A. C. Miller, Daniel P. Wang, Qian Whiteley, Marvin Lamont, Richard J. Hackett, Murray Front Microbiol Microbiology Many bacterial infections involve polymicrobial communities in which constituent organisms are synergistically pathogenic. Periodontitis, a commonly occurring chronic inflammatory disorder, is induced by multispecies bacterial communities. The periodontal keystone pathogen Porphyromonas gingivalis and the accessory pathogen Streptococcus gordonii exhibit polymicrobial synergy in animal models of disease. Mechanisms of co-adhesion and community formation by P. gingivalis and S. gordonii are well-established; however, little is known regarding the basis for increased pathogenicity. In this study we used time-coursed RNA-Seq to comprehensively and quantitatively examine the dynamic transcriptional landscape of P. gingivalis in a model consortium with S. gordonii. Genes encoding a number of potential virulence determinants had higher relative mRNA levels in the context of dual species model communities than P. gingivalis alone, including adhesins, the Type IX secretion apparatus, and tetratricopeptide repeat (TPR) motif proteins. In contrast, genes encoding conjugation systems and many of the stress responses showed lower levels of expression in P. gingivalis. A notable exception to reduced abundance of stress response transcripts was the genes encoding components of the oxidative stress-related OxyR regulon, indicating an adaptation of P. gingivalis to detoxify peroxide produced by the streptococcus. Collectively, the results are consistent with evolutionary adaptation of P. gingivalis to a polymicrobial oral environment, one outcome of which is increased pathogenic potential. Frontiers Media S.A. 2017-02-28 /pmc/articles/PMC5329018/ /pubmed/28293219 http://dx.doi.org/10.3389/fmicb.2017.00261 Text en Copyright © 2017 Hendrickson, Beck, Miller, Wang, Whiteley, Lamont and Hackett. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hendrickson, Erik L.
Beck, David A. C.
Miller, Daniel P.
Wang, Qian
Whiteley, Marvin
Lamont, Richard J.
Hackett, Murray
Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
title Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
title_full Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
title_fullStr Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
title_full_unstemmed Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
title_short Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
title_sort insights into dynamic polymicrobial synergy revealed by time-coursed rna-seq
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5329018/
https://www.ncbi.nlm.nih.gov/pubmed/28293219
http://dx.doi.org/10.3389/fmicb.2017.00261
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