Corncob structures in dental plaque reveal microhabitat taxon specificity
Abstract 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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-09-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01323-x |
| _version_ | 1828418781049782272 |
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| author | Viviana Morillo-Lopez Alexandra Sjaarda Imon Islam Gary G. Borisy Jessica L. Mark Welch |
| author_facet | Viviana Morillo-Lopez Alexandra Sjaarda Imon Islam Gary G. Borisy Jessica L. Mark Welch |
| author_sort | Viviana Morillo-Lopez |
| collection | DOAJ |
| description | Abstract 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. Video Abstract |
| first_indexed | 2024-12-10T14:42:19Z |
| format | Article |
| id | doaj.art-39d01d5851fe404bb8c8147622a1d48b |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-10T14:42:19Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-39d01d5851fe404bb8c8147622a1d48b2022-12-22T01:44:39ZengBMCMicrobiome2049-26182022-09-0110111410.1186/s40168-022-01323-xCorncob structures in dental plaque reveal microhabitat taxon specificityViviana Morillo-Lopez0Alexandra Sjaarda1Imon Islam2Gary G. Borisy3Jessica L. Mark Welch4Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryJosephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryJosephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryDepartment of Microbiology, The Forsyth InstituteJosephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryAbstract 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. Video Abstracthttps://doi.org/10.1186/s40168-022-01323-xOral microbiomeBiogeographyFluorescence in situ hybridizationFISHMicroscopyImaging |
| spellingShingle | Viviana Morillo-Lopez Alexandra Sjaarda Imon Islam Gary G. Borisy Jessica L. Mark Welch Corncob structures in dental plaque reveal microhabitat taxon specificity Microbiome Oral microbiome Biogeography Fluorescence in situ hybridization FISH Microscopy Imaging |
| 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 | Oral microbiome Biogeography Fluorescence in situ hybridization FISH Microscopy Imaging |
| url | https://doi.org/10.1186/s40168-022-01323-x |
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