Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment

ABSTRACT Periodontitis is a polymicrobial infectious disease that causes breakdown of the periodontal ligament and alveolar bone. We employed a meta-omics approach that included microbial 16S rRNA amplicon sequencing, shotgun metagenomics, and tandem mass spectrometry to analyze sub- and supragingiv...

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Autores principales:	Katy J. Califf, Karen Schwarzberg-Lipson, Neha Garg, Sean M. Gibbons, J. Gregory Caporaso, Jørgen Slots, Chloe Cohen, Pieter C. Dorrestein, Scott T. Kelley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	16S rRNA diagnostics metabolome microbiome molecular networking periodontal disease Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/15579f6ee0144f64804f3dbe1b2957a8
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spelling	oai:doaj.org-article:15579f6ee0144f64804f3dbe1b2957a82021-12-02T18:15:43ZMulti-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment10.1128/mSystems.00016-172379-5077https://doaj.org/article/15579f6ee0144f64804f3dbe1b2957a82017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00016-17https://doaj.org/toc/2379-5077ABSTRACT Periodontitis is a polymicrobial infectious disease that causes breakdown of the periodontal ligament and alveolar bone. We employed a meta-omics approach that included microbial 16S rRNA amplicon sequencing, shotgun metagenomics, and tandem mass spectrometry to analyze sub- and supragingival biofilms in adults with chronic periodontitis pre- and posttreatment with 0.25% sodium hypochlorite. Microbial samples were collected with periodontal curettes from 3- to 12-mm-deep periodontal pockets at the baseline and at 2 weeks and 3 months. All data types showed high interpersonal variability, and there was a significant correlation between phylogenetic diversity and pocket depth at the baseline and a strong correlation (rho = 0.21; P = 0.008) between metabolite diversity and maximum pocket depth (MPD). Analysis of subgingival baseline samples (16S rRNA and shotgun metagenomics) found positive correlations between abundances of particular bacterial genera and MPD, including Porphyromonas, Treponema, Tannerella, and Desulfovibrio species and unknown taxon SHD-231. At 2 weeks posttreatment, we observed an almost complete turnover in the bacterial genera (16S rRNA) and species (shotgun metagenomics) correlated with MPD. Among the metabolites detected, the medians of the 20 most abundant metabolites were significantly correlated with MPD pre- and posttreatment. Finally, tests of periodontal biofilm community instability found markedly higher taxonomic instability in patients who did not improve posttreatment than in patients who did improve (UniFrac distances; t = −3.59; P = 0.002). Interestingly, the opposite pattern occurred in the metabolic profiles (Bray-Curtis; t = 2.42; P = 0.02). Our results suggested that multi-omics approaches, and metabolomics analysis in particular, could enhance treatment prediction and reveal patients most likely to improve posttreatment. IMPORTANCE Periodontal disease affects the majority of adults worldwide and has been linked to numerous systemic diseases. Despite decades of research, the reasons for the substantial differences among periodontitis patients in disease incidence, progressivity, and response to treatment remain poorly understood. While deep sequencing of oral bacterial communities has greatly expanded our comprehension of the microbial diversity of periodontal disease and identified associations with healthy and disease states, predicting treatment outcomes remains elusive. Our results suggest that combining multiple omics approaches enhances the ability to differentiate among disease states and determine differential effects of treatment, particularly with the addition of metabolomic information. Furthermore, multi-omics analysis of biofilm community instability indicated that these approaches provide new tools for investigating the ecological dynamics underlying the progressive periodontal disease process.Katy J. CaliffKaren Schwarzberg-LipsonNeha GargSean M. GibbonsJ. Gregory CaporasoJørgen SlotsChloe CohenPieter C. DorresteinScott T. KelleyAmerican Society for Microbiologyarticle16S rRNAdiagnosticsmetabolomemicrobiomemolecular networkingperiodontal diseaseMicrobiologyQR1-502ENmSystems, Vol 2, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	16S rRNA diagnostics metabolome microbiome molecular networking periodontal disease Microbiology QR1-502
spellingShingle	16S rRNA diagnostics metabolome microbiome molecular networking periodontal disease Microbiology QR1-502 Katy J. Califf Karen Schwarzberg-Lipson Neha Garg Sean M. Gibbons J. Gregory Caporaso Jørgen Slots Chloe Cohen Pieter C. Dorrestein Scott T. Kelley Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment
description	ABSTRACT Periodontitis is a polymicrobial infectious disease that causes breakdown of the periodontal ligament and alveolar bone. We employed a meta-omics approach that included microbial 16S rRNA amplicon sequencing, shotgun metagenomics, and tandem mass spectrometry to analyze sub- and supragingival biofilms in adults with chronic periodontitis pre- and posttreatment with 0.25% sodium hypochlorite. Microbial samples were collected with periodontal curettes from 3- to 12-mm-deep periodontal pockets at the baseline and at 2 weeks and 3 months. All data types showed high interpersonal variability, and there was a significant correlation between phylogenetic diversity and pocket depth at the baseline and a strong correlation (rho = 0.21; P = 0.008) between metabolite diversity and maximum pocket depth (MPD). Analysis of subgingival baseline samples (16S rRNA and shotgun metagenomics) found positive correlations between abundances of particular bacterial genera and MPD, including Porphyromonas, Treponema, Tannerella, and Desulfovibrio species and unknown taxon SHD-231. At 2 weeks posttreatment, we observed an almost complete turnover in the bacterial genera (16S rRNA) and species (shotgun metagenomics) correlated with MPD. Among the metabolites detected, the medians of the 20 most abundant metabolites were significantly correlated with MPD pre- and posttreatment. Finally, tests of periodontal biofilm community instability found markedly higher taxonomic instability in patients who did not improve posttreatment than in patients who did improve (UniFrac distances; t = −3.59; P = 0.002). Interestingly, the opposite pattern occurred in the metabolic profiles (Bray-Curtis; t = 2.42; P = 0.02). Our results suggested that multi-omics approaches, and metabolomics analysis in particular, could enhance treatment prediction and reveal patients most likely to improve posttreatment. IMPORTANCE Periodontal disease affects the majority of adults worldwide and has been linked to numerous systemic diseases. Despite decades of research, the reasons for the substantial differences among periodontitis patients in disease incidence, progressivity, and response to treatment remain poorly understood. While deep sequencing of oral bacterial communities has greatly expanded our comprehension of the microbial diversity of periodontal disease and identified associations with healthy and disease states, predicting treatment outcomes remains elusive. Our results suggest that combining multiple omics approaches enhances the ability to differentiate among disease states and determine differential effects of treatment, particularly with the addition of metabolomic information. Furthermore, multi-omics analysis of biofilm community instability indicated that these approaches provide new tools for investigating the ecological dynamics underlying the progressive periodontal disease process.
format	article
author	Katy J. Califf Karen Schwarzberg-Lipson Neha Garg Sean M. Gibbons J. Gregory Caporaso Jørgen Slots Chloe Cohen Pieter C. Dorrestein Scott T. Kelley
author_facet	Katy J. Califf Karen Schwarzberg-Lipson Neha Garg Sean M. Gibbons J. Gregory Caporaso Jørgen Slots Chloe Cohen Pieter C. Dorrestein Scott T. Kelley
author_sort	Katy J. Califf
title	Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment
title_short	Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment
title_full	Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment
title_fullStr	Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment
title_full_unstemmed	Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment
title_sort	multi-omics analysis of periodontal pocket microbial communities pre- and posttreatment
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/15579f6ee0144f64804f3dbe1b2957a8
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Multi-omics Analysis of Periodontal Pocket Microbial Communities Pre- and Posttreatment

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