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.

Complex polymicrobial biofilm communities are abundant in nature particularly in the human oral cavity where their composition and fitness can affect health. While the study of these communities during disease is essential and prevalent, little is known about interactions within the healthy plaque community. Here we describe interactions between two of the most abundant species in this healthy microbiome, Haemophilus parainfluenzae and Streptococcus mitis. We discovered that H. parainfluenzae typically exists adjacent to mitis group streptococci in vivo with which it is also positively correlated based on microbiome data. By comparing in vitro coculture data to ex vivo microscopy we revealed that this co-occurrence is density dependent and further influenced by H2O2 production. We discovered that H. parainfluenzae utilizes a more redundant, multifactorial response to H2O2 than related microorganisms and that this system’s integrity enhances streptococcal fitness. Our results indicate that mitis group streptococci are likely the in vivo source of NAD for H. parainfluenzae and also evoke patterns of carbon utilization in vitro for H. parainfluenzae similar to those observed in vivo. Our findings describe mechanistic interactions between two of the most abundant and prevalent members of healthy supragingival plaque that contribute to their in vivo survival.

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 possess 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 microhabitat specialization involving these taxa as well. Conclusions The spatial organization we observed in corncobs suggests that each of the microbial participants is capable of interacting 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.

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