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Adherence to Streptococci Facilitates Fusobacterium nucleatum Integration into an Oral Microbial Community

  • Environmental Microbiology
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Abstract

The development of multispecies oral microbial communities involves complex intra- and interspecies interactions at various levels. The ability to adhere to the resident bacteria or the biofilm matrix and overcome community resistance are among the key factors that determine whether a bacterium can integrate into a community. Fusobacterium nucleatum is a prevalent Gram-negative oral bacterial species that is able to adhere to a variety of oral microbes and has been implicated in playing an important role in the establishment of multispecies oral microbial community. However, the majority of experiments thus far has focused on the physical adherence between two species as measured by in vitro co-aggregation assays, while the community-based effects on the integration of F. nucleatum into multispecies microbial community remains to be investigated. In this study, we focus on community integration of F. nucleatum. We demonstrated using an established in vitro mice oral microbiota (O-mix) that the viability of F. nucleatum was significantly reduced upon addition to the O-mix due to cell contact-dependent induction of hydrogen peroxide (H2O2) production by oral community. Interestingly, this inhibitory effect was significantly alleviated when F. nucleatum was allowed to adhere to its known interacting partner species (such as Streptococcus sanguinis) prior to addition. Furthermore, this aggregate formation-dependent protection was absent in the F. nucleatum mutant strain ΔFn1526 that is unable to bind to a number of Gram-positive species. More importantly, this protective effect was also observed during integration of F. nucleatum into a human salivary microbial community (S-mix). These results suggest that by adhering to other oral microbes, F. nucleatum is able to mask the surface components that are recognized by H2O2 producing oral community members. This evasion strategy prevents detection by antagonistic oral bacteria and allows integration into the developing oral microbial community.

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Acknowledgments

The study was supported by US National Institutes of Health (NIH) Grants (DE020102 and DE021108) and National Basic Research Program of China (2011CB512108).

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Authors and Affiliations

  1. UCLA School of Dentistry, 10833 Le Conte Avenue, CHS 20-114, Los Angeles, CA, 90095-1668, USA

    Xuesong He, Wei Hu, Lihong Guo, Wenyuan Shi & Renate Lux

  2. C3 Jian Inc., Inglewood, CA, USA

    Christopher W. Kaplan & Wenyuan Shi

  3. State Key Laboratory of Microbial Technology, School of Life Science, Shandong University, Jinan, Shandong, 250100, China

    Wei Hu

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  1. Xuesong He
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  2. Wei Hu
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  3. Christopher W. Kaplan
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  6. Renate Lux
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Correspondence to Renate Lux.

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Xuesong He and Wei Hu contributed equally to this work.

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He, X., Hu, W., Kaplan, C.W. et al. Adherence to Streptococci Facilitates Fusobacterium nucleatum Integration into an Oral Microbial Community. Microb Ecol 63, 532–542 (2012). https://doi.org/10.1007/s00248-011-9989-2

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  • DOI: https://doi.org/10.1007/s00248-011-9989-2

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