Abstract
Periodontitis has a polymicrobial etiology within the framework of a complex microbial ecosystem. With advances in sequencing technologies, comprehensive studies to elucidate bacterial community differences have recently become possible. We used 454 sequencing of 16S rRNA genes to compare subgingival bacterial communities from 29 periodontally healthy controls and 29 subjects with chronic periodontitis. Amplicons from both the V1-2 and V4 regions of the 16S gene were sequenced, yielding 1 393 579 sequences. They were identified by BLAST against a curated oral 16S database, and mapped to 16 phyla, 106 genera, and 596 species. 81% of sequences could be mapped to cultivated species. Differences between health- and periodontitis-associated bacterial communities were observed at all phylogenetic levels, and UniFrac and principal coordinates analysis showed distinct community profiles in health and disease. Community diversity was higher in disease, and 123 species were identified that were significantly more abundant in disease, and 53 in health. Spirochaetes, Synergistetes and Bacteroidetes were more abundant in disease, whereas the Proteobacteria were found at higher levels in healthy controls. Within the phylum Firmicutes, the class Bacilli was health-associated, whereas the Clostridia, Negativicutes and Erysipelotrichia were associated with disease. These results implicate a number of taxa that will be targets for future research. Some, such as Filifactor alocis and many Spirochetes were represented by a large fraction of sequences as compared with previously identified targets. Elucidation of these differences in community composition provides a basis for further understanding the pathogenesis of periodontitis.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ . (1990). Basic local alignment search tool. J Mol Biol 215: 403–410.
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2009). The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141–D145.
Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH et al. (2010). The human oral microbiome. J Bacteriol 192: 5002–5017.
Griffen AL, Beall CJ, Firestone ND, Gross EL, DiFranco JM, Hardman JH et al. (2011). CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS ONE 6: e19051.
Gross EL, Leys EJ, Gasparovich SR, Firestone ND, Schwartzbaum JA, Janies DA et al. (2010). Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 48: 4121–4128.
Hamady M, Lozupone C, Knight R . (2009). Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17–27.
Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC et al. (2008). Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87: 1016–1020.
Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ . (2003). New bacterial species associated with chronic periodontitis. J Dent Res 82: 338–344.
Kumar PS, Griffen AL, Moeschberger ML, Leys EJ . (2005). Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiology 43: 3944–3955.
Kumar PS, Leys EJ, Bryk JM, Martinez FJ, Moeschberger ML, Griffen AL . (2006). Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J Clin Microbiol 44: 3665–3673.
Lane D . (1991). 16S/23S rRNA sequencing. In: Stackebrant E, Goodfellow M (eds). Nucleic Acid Techniques in Bacterial Systematics. John Wiley & Sons: New York, pp 115–175.
Letunic I, Bork P . (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127–128.
Marsh PD . (2003). Are dental diseases examples of ecological catastrophes? Microbiology 149: 279–294.
Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA et al. (2001). Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770–3783.
Pushalkar S, Mane SP, Ji X, Li Y, Evans C, Crasta OR et al. (2011). Microbial diversity in saliva of oral squamous cell carcinoma. FEMS Immunol Med Microbiol 61: 269–277.
Scannapieco FA, Dasanayake AP, Chhun N . (2010). Does periodontal therapy reduce the risk for systemic diseases? Dent Clin North Am 54: 163–181.
Shannon CE . (1948). A mathematical theory of communication. Bell Syst Tech J 27: 379–423 623–656.
Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent Jr RL . (1998). Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134–144.
Wade WG . (2011). Has the use of molecular methods for the characterization of the human oral microbiome changed our understanding of the role of bacteria in the pathogenesis of periodontal disease? J Clin Periodontol 38 Suppl 11: 7–16.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ . (1991). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697–703.
Zaura E, Keijser BJ, Huse SM, Crielaard W . (2009). Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol 9: 259.
Acknowledgements
This work was supported by NIDCR Grant no. R01DE010467. We would like to thank Danny Dayeh, James DiFranco, Jennifer Harris and Migun Shakya for technical support. JHC, ZKY and MP were sponsored by the US Department of Energy Office of Science, Biological and Environmental Research programs at Oak Ridge National Laboratory (ORNL). ORNL is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC05-00OR22725.
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Griffen, A., Beall, C., Campbell, J. et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6, 1176–1185 (2012). https://doi.org/10.1038/ismej.2011.191
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DOI: https://doi.org/10.1038/ismej.2011.191
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