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Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA

Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and charact...

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Autores principales: Rostami, Nadia, Shields, Robert C., Serrage, Hannah J., Lawler, Catherine, Brittan, Jane L., Yassin, Sufian, Ahmed, Halah, Treumann, Achim, Thompson, Paul, Waldron, Kevin J., Nobbs, Angela H., Jakubovics, Nicholas S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744736/
https://www.ncbi.nlm.nih.gov/pubmed/36509765
http://dx.doi.org/10.1038/s41522-022-00359-z
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author Rostami, Nadia
Shields, Robert C.
Serrage, Hannah J.
Lawler, Catherine
Brittan, Jane L.
Yassin, Sufian
Ahmed, Halah
Treumann, Achim
Thompson, Paul
Waldron, Kevin J.
Nobbs, Angela H.
Jakubovics, Nicholas S.
author_facet Rostami, Nadia
Shields, Robert C.
Serrage, Hannah J.
Lawler, Catherine
Brittan, Jane L.
Yassin, Sufian
Ahmed, Halah
Treumann, Achim
Thompson, Paul
Waldron, Kevin J.
Nobbs, Angela H.
Jakubovics, Nicholas S.
author_sort Rostami, Nadia
collection PubMed
description Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms.
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spelling pubmed-97447362022-12-14 Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA Rostami, Nadia Shields, Robert C. Serrage, Hannah J. Lawler, Catherine Brittan, Jane L. Yassin, Sufian Ahmed, Halah Treumann, Achim Thompson, Paul Waldron, Kevin J. Nobbs, Angela H. Jakubovics, Nicholas S. NPJ Biofilms Microbiomes Article Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms. Nature Publishing Group UK 2022-12-12 /pmc/articles/PMC9744736/ /pubmed/36509765 http://dx.doi.org/10.1038/s41522-022-00359-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Rostami, Nadia
Shields, Robert C.
Serrage, Hannah J.
Lawler, Catherine
Brittan, Jane L.
Yassin, Sufian
Ahmed, Halah
Treumann, Achim
Thompson, Paul
Waldron, Kevin J.
Nobbs, Angela H.
Jakubovics, Nicholas S.
Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA
title Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA
title_full Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA
title_fullStr Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA
title_full_unstemmed Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA
title_short Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA
title_sort interspecies competition in oral biofilms mediated by streptococcus gordonii extracellular deoxyribonuclease ssna
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744736/
https://www.ncbi.nlm.nih.gov/pubmed/36509765
http://dx.doi.org/10.1038/s41522-022-00359-z
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