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      Functional biomarkers for chronic periodontitis and insights into the roles of Prevotella nigrescens and Fusobacterium nucleatum; a metatranscriptome analysis

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          Abstract

          Background/Objectives:

          Periodontitis is the most prevalent inflammatory disease worldwide and is caused by a dysbiotic subgingival biofilm. Here we used metatranscriptomics to determine the functional shift from health to periodontitis, the response of individual species to dysbiosis and to discover biomarkers.

          Methods:

          Sixteen individuals were studied, from which six were diagnosed with chronic periodontitis. Illumina sequencing of the total messenger RNA (mRNA) yielded ~42 million reads per sample. A total of 324 human oral taxon phylotypes and 366,055 open reading frames from the HOMD database reference genomes were detected.

          Results:

          The transcriptionally active community shifted from Bacilli and Actinobacteria in health to Bacteroidia, Deltaproteobacteria, Spirochaetes and Synergistetes in periodontitis. Clusters of orthologous groups (COGs) related to carbohydrate transport and catabolism dominated in health, whereas protein degradation and amino acid catabolism dominated in disease. The LEfSe, random forest and support vector machine methods were applied to the 2,000 most highly expressed genes and discovered the three best functional biomarkers, namely haem binding protein HmuY from Porphyromonas gingivalis, flagellar filament core protein FlaB3 from Treponema denticola, and repeat protein of unknown function from Filifactor alocis. They predicted the diagnosis correctly for 14 from 16 individuals, and when applied to an independent study misclassified one out of six subjects only. Prevotella nigrescens shifted from commensalism to virulence by upregulating the expression of metalloproteases and the haem transporter. Expression of genes for the synthesis of the cytotoxic short-chain fatty acid butyrate was observed by Fusobacterium nucleatum under all conditions. Four additional species contributed to butyrate synthesis in periodontitis and they used an additional pathway.

          Conclusion:

          Gene biomarkers of periodontitis are highly predictive. The pro-inflammatory role of F. nucelatum is not related to butyrate synthesis.

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          Most cited references33

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          Periodontitis: a polymicrobial disruption of host homeostasis.

          Richard Darveau (2010)
          Periodontitis, or gum disease, affects millions of people each year. Although it is associated with a defined microbial composition found on the surface of the tooth and tooth root, the contribution of bacteria to disease progression is poorly understood. Commensal bacteria probably induce a protective response that prevents the host from developing disease. However, several bacterial species found in plaque (the 'red-complex' bacteria: Porphyromonas gingivalis, Tannerella forsythia and Treponema denticola) use various mechanisms to interfere with host defence mechanisms. Furthermore, disease may result from 'community-based' attack on the host. Here, I describe the interaction of the host immune system with the oral bacteria in healthy states and in diseased states.
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            The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation.

            Loreto Abusleme, Amanda Dupuy, Nicolás DUTZAN … (2013)
            The goals of this study were to better understand the ecology of oral subgingival communities in health and periodontitis and elucidate the relationship between inflammation and the subgingival microbiome. Accordingly, we used 454-pyrosequencing of 16S rRNA gene libraries and quantitative PCR to characterize the subgingival microbiome of 22 subjects with chronic periodontitis. Each subject was sampled at two sites with similar periodontal destruction but differing in the presence of bleeding, a clinical indicator of increased inflammation. Communities in periodontitis were also compared with those from 10 healthy individuals. In periodontitis, presence of bleeding was not associated with different α-diversity or with a distinct microbiome, however, bleeding sites showed higher total bacterial load. In contrast, communities in health and periodontitis largely differed, with higher diversity and biomass in periodontitis. Shifts in community structure from health to periodontitis resembled ecological succession, with emergence of newly dominant taxa in periodontitis without replacement of primary health-associated species. That is, periodontitis communities had higher proportions of Spirochetes, Synergistetes, Firmicutes and Chloroflexi, among other taxa, while the proportions of Actinobacteria, particularly Actinomyces, were higher in health. Total Actinomyces load, however, remained constant from health to periodontitis. Moreover, an association existed between biomass and community structure in periodontitis, with the proportion of specific taxa correlating with bacterial load. Our study provides a global-scale framework for the ecological events in subgingival communities that underline the development of periodontitis. The association, in periodontitis, between inflammation, community biomass and community structure and their role in disease progression warrant further investigation.
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              From the gut to the peripheral tissues: the multiple effects of butyrate.

              P Guilloteau, L. Martin, V Eeckhaut … (2010)
              Butyrate is a natural substance present in biological liquids and tissues. The present paper aims to give an update on the biological role of butyrate in mammals, when it is naturally produced by the gastrointestinal microbiota or orally ingested as a feed additive. Recent data concerning butyrate production delivery as well as absorption by the colonocytes are reported. Butyrate cannot be detected in the peripheral blood, which indicates fast metabolism in the gut wall and/or in the liver. In physiological conditions, the increase in performance in animals could be explained by the increased nutrient digestibility, the stimulation of the digestive enzyme secretions, a modification of intestinal luminal microbiota and an improvement of the epithelial integrity and defence systems. In the digestive tract, butyrate can act directly (upper gastrointestinal tract or hindgut) or indirectly (small intestine) on tissue development and repair. Direct trophic effects have been demonstrated mainly by cell proliferation studies, indicating a faster renewal of necrotic areas. Indirect actions of butyrate are believed to involve the hormono-neuro-immuno system. Butyrate has also been implicated in down-regulation of bacteria virulence, both by direct effects on virulence gene expression and by acting on cell proliferation of the host cells. In animal production, butyrate is a helpful feed additive, especially when ingested soon after birth, as it enhances performance and controls gut health disorders caused by bacterial pathogens. Such effects could be considered for new applications in human nutrition.
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                Author and article information

                Journal
                Journal ID (nlm-ta): NPJ Biofilms Microbiomes
                Journal ID (iso-abbrev): NPJ Biofilms Microbiomes
                Title: NPJ Biofilms and Microbiomes
                Publisher: Nature Publishing Group
                ISSN (Electronic): 2055-5008
                Publication date (Electronic): 23 September 2015
                Publication date Collection: 2015
                Volume: 1
                Page: 15017
                Affiliations
                [1 ] Research Group Microbial Communication, Department of Molecular Infection Biology, Helmholtz Centre for Infection Research (HZI) , Braunschweig, Germany
                [2 ] Genome Analytics, Helmholtz Centre for Infection Research , Braunschweig, Germany
                [3 ] Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH) , Neuherberg, Germany
                [4 ] Department of Conservative Dentistry, Ludwig-Maximilians-University , München, Germany
                Author notes
                [5]

                These authors contributed equally to the supervision of SPS.

                This study was designed by IW-D. CM and JK provided the clinical samples. RNA extraction and enrichment was performed by SPS. SB prepared cDNA libraries and performed Illumina sequencing. Bioinformatics analyses were performed by Z-LD, JT and MJ. Data interpretation and visualisation were done by SPS, Z-LD, HS and IW-D. SPS, HS and IW-D wrote the manuscript.

                Article
                Publisher Item ID: npjbiofilms201517
                DOI: 10.1038/npjbiofilms.2015.17
                PMC ID: 5515211
                SO-VID: 71628be0-a150-449e-ad41-f87e8f1bee29
                Copyright © Copyright © 2015 Nanyang Technological University/Macmillan Publishers Limited
                License:

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                Date received : 19 May 2015
                Date revision received : 07 August 2015
                Date accepted : 20 August 2015
                Categories
                Subject: Article

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