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Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses

Porphyromonas gingivalis and Treponema denticola are strongly associated with chronic periodontitis. These bacteria have been co-localized in subgingival plaque and demonstrated to exhibit symbiosis in growth in vitro and synergistic virulence upon co-infection in animal models of disease. Here we s...

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Autores principales: Tan, Kheng H., Seers, Christine A., Dashper, Stuart G., Mitchell, Helen L., Pyke, James S., Meuric, Vincent, Slakeski, Nada, Cleal, Steven M., Chambers, Jenny L., McConville, Malcolm J., Reynolds, Eric C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3946380/
https://www.ncbi.nlm.nih.gov/pubmed/24603978
http://dx.doi.org/10.1371/journal.ppat.1003955
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author Tan, Kheng H.
Seers, Christine A.
Dashper, Stuart G.
Mitchell, Helen L.
Pyke, James S.
Meuric, Vincent
Slakeski, Nada
Cleal, Steven M.
Chambers, Jenny L.
McConville, Malcolm J.
Reynolds, Eric C.
author_facet Tan, Kheng H.
Seers, Christine A.
Dashper, Stuart G.
Mitchell, Helen L.
Pyke, James S.
Meuric, Vincent
Slakeski, Nada
Cleal, Steven M.
Chambers, Jenny L.
McConville, Malcolm J.
Reynolds, Eric C.
author_sort Tan, Kheng H.
collection PubMed
description Porphyromonas gingivalis and Treponema denticola are strongly associated with chronic periodontitis. These bacteria have been co-localized in subgingival plaque and demonstrated to exhibit symbiosis in growth in vitro and synergistic virulence upon co-infection in animal models of disease. Here we show that during continuous co-culture a P. gingivalis:T. denticola cell ratio of 6∶1 was maintained with a respective increase of 54% and 30% in cell numbers when compared with mono-culture. Co-culture caused significant changes in global gene expression in both species with altered expression of 184 T. denticola and 134 P. gingivalis genes. P. gingivalis genes encoding a predicted thiamine biosynthesis pathway were up-regulated whilst genes involved in fatty acid biosynthesis were down-regulated. T. denticola genes encoding virulence factors including dentilisin and glycine catabolic pathways were significantly up-regulated during co-culture. Metabolic labeling using (13)C-glycine showed that T. denticola rapidly metabolized this amino acid resulting in the production of acetate and lactate. P. gingivalis may be an important source of free glycine for T. denticola as mono-cultures of P. gingivalis and T. denticola were found to produce and consume free glycine, respectively; free glycine production by P. gingivalis was stimulated by T. denticola conditioned medium and glycine supplementation of T. denticola medium increased final cell density 1.7-fold. Collectively these data show P. gingivalis and T. denticola respond metabolically to the presence of each other with T. denticola displaying responses that help explain enhanced virulence of co-infections.
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spelling pubmed-39463802014-03-12 Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses Tan, Kheng H. Seers, Christine A. Dashper, Stuart G. Mitchell, Helen L. Pyke, James S. Meuric, Vincent Slakeski, Nada Cleal, Steven M. Chambers, Jenny L. McConville, Malcolm J. Reynolds, Eric C. PLoS Pathog Research Article Porphyromonas gingivalis and Treponema denticola are strongly associated with chronic periodontitis. These bacteria have been co-localized in subgingival plaque and demonstrated to exhibit symbiosis in growth in vitro and synergistic virulence upon co-infection in animal models of disease. Here we show that during continuous co-culture a P. gingivalis:T. denticola cell ratio of 6∶1 was maintained with a respective increase of 54% and 30% in cell numbers when compared with mono-culture. Co-culture caused significant changes in global gene expression in both species with altered expression of 184 T. denticola and 134 P. gingivalis genes. P. gingivalis genes encoding a predicted thiamine biosynthesis pathway were up-regulated whilst genes involved in fatty acid biosynthesis were down-regulated. T. denticola genes encoding virulence factors including dentilisin and glycine catabolic pathways were significantly up-regulated during co-culture. Metabolic labeling using (13)C-glycine showed that T. denticola rapidly metabolized this amino acid resulting in the production of acetate and lactate. P. gingivalis may be an important source of free glycine for T. denticola as mono-cultures of P. gingivalis and T. denticola were found to produce and consume free glycine, respectively; free glycine production by P. gingivalis was stimulated by T. denticola conditioned medium and glycine supplementation of T. denticola medium increased final cell density 1.7-fold. Collectively these data show P. gingivalis and T. denticola respond metabolically to the presence of each other with T. denticola displaying responses that help explain enhanced virulence of co-infections. Public Library of Science 2014-03-06 /pmc/articles/PMC3946380/ /pubmed/24603978 http://dx.doi.org/10.1371/journal.ppat.1003955 Text en © 2014 Tan 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
Tan, Kheng H.
Seers, Christine A.
Dashper, Stuart G.
Mitchell, Helen L.
Pyke, James S.
Meuric, Vincent
Slakeski, Nada
Cleal, Steven M.
Chambers, Jenny L.
McConville, Malcolm J.
Reynolds, Eric C.
Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses
title Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses
title_full Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses
title_fullStr Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses
title_full_unstemmed Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses
title_short Porphyromonas gingivalis and Treponema denticola Exhibit Metabolic Symbioses
title_sort porphyromonas gingivalis and treponema denticola exhibit metabolic symbioses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3946380/
https://www.ncbi.nlm.nih.gov/pubmed/24603978
http://dx.doi.org/10.1371/journal.ppat.1003955
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