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Corncob structures in dental plaque reveal microhabitat taxon specificity

BACKGROUND: The human mouth is a natural laboratory for studying how bacterial communities differ across habitats. Different bacteria colonize different surfaces in the mouth—teeth, tongue dorsum, and keratinized and non-keratinized epithelia—despite the short physical distance between these habitat...

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Autores principales: Morillo-Lopez, Viviana, Sjaarda, Alexandra, Islam, Imon, Borisy, Gary G., Mark Welch, Jessica L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446765/
https://www.ncbi.nlm.nih.gov/pubmed/36064650
http://dx.doi.org/10.1186/s40168-022-01323-x
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author Morillo-Lopez, Viviana
Sjaarda, Alexandra
Islam, Imon
Borisy, Gary G.
Mark Welch, Jessica L.
author_facet Morillo-Lopez, Viviana
Sjaarda, Alexandra
Islam, Imon
Borisy, Gary G.
Mark Welch, Jessica L.
author_sort Morillo-Lopez, Viviana
collection PubMed
description BACKGROUND: The human mouth is a natural laboratory for studying how bacterial communities differ across habitats. Different bacteria colonize different surfaces in the mouth—teeth, tongue dorsum, and keratinized and non-keratinized epithelia—despite the short physical distance between these habitats and their connection through saliva. We sought to determine whether more tightly defined microhabitats might have more tightly defined sets of resident bacteria. A microhabitat may be characterized, for example, as the space adjacent to a particular species of bacterium. Corncob structures of dental plaque, consisting of coccoid bacteria bound to filaments of Corynebacterium cells, present an opportunity to analyze the community structure of one such well-defined microhabitat within a complex natural biofilm. Here, we investigate by fluorescence in situ hybridization and spectral imaging the composition of the cocci decorating the filaments. RESULTS: The range of taxa observed in corncobs was limited to a small subset of the taxa present in dental plaque. Among four major groups of dental plaque streptococci, two were the major constituents of corncobs, including one that was the most abundant Streptococcus species in corncobs despite being relatively rare in dental plaque overall. Images showed both Streptococcus types in corncobs in all individual donors, suggesting that the taxa have different ecological roles or that mechanisms exist for stabilizing the persistence of functionally redundant taxa in the population. Direct taxon-taxon interactions were observed not only between the Streptococcus cells and the central corncob filament but also between Streptococcus cells and the limited subset of other plaque bacteria detected in the corncobs, indicating species ensembles involving these taxa as well. CONCLUSIONS: The spatial organization we observed in corncobs suggests that each of the microbial participants can interact with multiple, albeit limited, potential partners, a feature that may encourage the long-term stability of the community. Additionally, our results suggest the general principle that a precisely defined microhabitat will be inhabited by a small and well-defined set of microbial taxa. Thus, our results are important for understanding the structure and organizing principles of natural biofilms and lay the groundwork for future work to modulate and control biofilms for human health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01323-x.
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spelling pubmed-94467652022-09-07 Corncob structures in dental plaque reveal microhabitat taxon specificity Morillo-Lopez, Viviana Sjaarda, Alexandra Islam, Imon Borisy, Gary G. Mark Welch, Jessica L. Microbiome Research BACKGROUND: The human mouth is a natural laboratory for studying how bacterial communities differ across habitats. Different bacteria colonize different surfaces in the mouth—teeth, tongue dorsum, and keratinized and non-keratinized epithelia—despite the short physical distance between these habitats and their connection through saliva. We sought to determine whether more tightly defined microhabitats might have more tightly defined sets of resident bacteria. A microhabitat may be characterized, for example, as the space adjacent to a particular species of bacterium. Corncob structures of dental plaque, consisting of coccoid bacteria bound to filaments of Corynebacterium cells, present an opportunity to analyze the community structure of one such well-defined microhabitat within a complex natural biofilm. Here, we investigate by fluorescence in situ hybridization and spectral imaging the composition of the cocci decorating the filaments. RESULTS: The range of taxa observed in corncobs was limited to a small subset of the taxa present in dental plaque. Among four major groups of dental plaque streptococci, two were the major constituents of corncobs, including one that was the most abundant Streptococcus species in corncobs despite being relatively rare in dental plaque overall. Images showed both Streptococcus types in corncobs in all individual donors, suggesting that the taxa have different ecological roles or that mechanisms exist for stabilizing the persistence of functionally redundant taxa in the population. Direct taxon-taxon interactions were observed not only between the Streptococcus cells and the central corncob filament but also between Streptococcus cells and the limited subset of other plaque bacteria detected in the corncobs, indicating species ensembles involving these taxa as well. CONCLUSIONS: The spatial organization we observed in corncobs suggests that each of the microbial participants can interact with multiple, albeit limited, potential partners, a feature that may encourage the long-term stability of the community. Additionally, our results suggest the general principle that a precisely defined microhabitat will be inhabited by a small and well-defined set of microbial taxa. Thus, our results are important for understanding the structure and organizing principles of natural biofilms and lay the groundwork for future work to modulate and control biofilms for human health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01323-x. BioMed Central 2022-09-05 /pmc/articles/PMC9446765/ /pubmed/36064650 http://dx.doi.org/10.1186/s40168-022-01323-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Morillo-Lopez, Viviana
Sjaarda, Alexandra
Islam, Imon
Borisy, Gary G.
Mark Welch, Jessica L.
Corncob structures in dental plaque reveal microhabitat taxon specificity
title Corncob structures in dental plaque reveal microhabitat taxon specificity
title_full Corncob structures in dental plaque reveal microhabitat taxon specificity
title_fullStr Corncob structures in dental plaque reveal microhabitat taxon specificity
title_full_unstemmed Corncob structures in dental plaque reveal microhabitat taxon specificity
title_short Corncob structures in dental plaque reveal microhabitat taxon specificity
title_sort corncob structures in dental plaque reveal microhabitat taxon specificity
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446765/
https://www.ncbi.nlm.nih.gov/pubmed/36064650
http://dx.doi.org/10.1186/s40168-022-01323-x
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