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Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms

Mixed species biofilms are shaped and influenced by interactions between species. In the oral cavity, dysbiosis of the microbiome leads to diseases such as periodontitis. Porphyromonas gingivalis is a keystone pathogen of periodontitis. In this study, we showed that polymicrobial biofilm formation p...

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Autores principales: Zhu, Bin, Macleod, Lorna C., Newsome, Eric, Liu, Jinlin, Xu, Ping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426879/
https://www.ncbi.nlm.nih.gov/pubmed/30894650
http://dx.doi.org/10.1038/s41598-019-41467-9
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author Zhu, Bin
Macleod, Lorna C.
Newsome, Eric
Liu, Jinlin
Xu, Ping
author_facet Zhu, Bin
Macleod, Lorna C.
Newsome, Eric
Liu, Jinlin
Xu, Ping
author_sort Zhu, Bin
collection PubMed
description Mixed species biofilms are shaped and influenced by interactions between species. In the oral cavity, dysbiosis of the microbiome leads to diseases such as periodontitis. Porphyromonas gingivalis is a keystone pathogen of periodontitis. In this study, we showed that polymicrobial biofilm formation promoted the tolerance of Porphyromonas gingivalis to oxidative stress under micro-aerobic conditions. The presence of Streptococcus sanguinis, an oral commensal bacterium, inhibited the survival of P. gingivalis in dual-species biofilms via the secretion of hydrogen peroxide (H(2)O(2)). Interestingly, this repression could be attenuated by the presence of Aggregatibacter actinomycetemcomitans in tri-species biofilms. It was also shown that the katA gene, encoding a cytoplasmic catalase in A. actinomycetemcomitans, was responsible for the reduction of H(2)O(2) produced by S. sanguinis, which consequently increased the biomass of P. gingivalis in tri-species biofilms. Collectively, these findings reveal that polymicrobial interactions play important roles in shaping bacterial community in biofilm. The existence of catalase producers may support the colonization of pathogens vulnerable to H(2)O(2), in the oral cavity. The catalase may be a potential drug target to aid in the prevention of periodontitis.
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spelling pubmed-64268792019-03-28 Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms Zhu, Bin Macleod, Lorna C. Newsome, Eric Liu, Jinlin Xu, Ping Sci Rep Article Mixed species biofilms are shaped and influenced by interactions between species. In the oral cavity, dysbiosis of the microbiome leads to diseases such as periodontitis. Porphyromonas gingivalis is a keystone pathogen of periodontitis. In this study, we showed that polymicrobial biofilm formation promoted the tolerance of Porphyromonas gingivalis to oxidative stress under micro-aerobic conditions. The presence of Streptococcus sanguinis, an oral commensal bacterium, inhibited the survival of P. gingivalis in dual-species biofilms via the secretion of hydrogen peroxide (H(2)O(2)). Interestingly, this repression could be attenuated by the presence of Aggregatibacter actinomycetemcomitans in tri-species biofilms. It was also shown that the katA gene, encoding a cytoplasmic catalase in A. actinomycetemcomitans, was responsible for the reduction of H(2)O(2) produced by S. sanguinis, which consequently increased the biomass of P. gingivalis in tri-species biofilms. Collectively, these findings reveal that polymicrobial interactions play important roles in shaping bacterial community in biofilm. The existence of catalase producers may support the colonization of pathogens vulnerable to H(2)O(2), in the oral cavity. The catalase may be a potential drug target to aid in the prevention of periodontitis. Nature Publishing Group UK 2019-03-20 /pmc/articles/PMC6426879/ /pubmed/30894650 http://dx.doi.org/10.1038/s41598-019-41467-9 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Zhu, Bin
Macleod, Lorna C.
Newsome, Eric
Liu, Jinlin
Xu, Ping
Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
title Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
title_full Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
title_fullStr Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
title_full_unstemmed Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
title_short Aggregatibacter actinomycetemcomitans mediates protection of Porphyromonas gingivalis from Streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
title_sort aggregatibacter actinomycetemcomitans mediates protection of porphyromonas gingivalis from streptococcus sanguinis hydrogen peroxide production in multi-species biofilms
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426879/
https://www.ncbi.nlm.nih.gov/pubmed/30894650
http://dx.doi.org/10.1038/s41598-019-41467-9
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