Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis

ABSTRACT Over half of adults experience gingivitis, a mild yet treatable form of periodontal disease caused by the overgrowth of oral microbes. Left untreated, gingivitis can progress to a more severe and irreversible disease, most commonly chronic periodontitis. While periodontal diseases are assoc...

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Autores principales:	Emily M. Nowicki, Raghav Shroff, Jacqueline A. Singleton, Diane E. Renaud, Debra Wallace, Julie Drury, Jolene Zirnheld, Brock Colleti, Andrew D. Ellington, Richard J. Lamont, David A. Scott, Marvin Whiteley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	dysbiosis gingivitis metatranscriptome oral microbiology periodontitis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cd490253441c4376b1cc114f8483fea9
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spelling	oai:doaj.org-article:cd490253441c4376b1cc114f8483fea92021-11-15T15:53:27ZMicrobiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis10.1128/mBio.00575-182150-7511https://doaj.org/article/cd490253441c4376b1cc114f8483fea92018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00575-18https://doaj.org/toc/2150-7511ABSTRACT Over half of adults experience gingivitis, a mild yet treatable form of periodontal disease caused by the overgrowth of oral microbes. Left untreated, gingivitis can progress to a more severe and irreversible disease, most commonly chronic periodontitis. While periodontal diseases are associated with a shift in the oral microbiota composition, it remains unclear how this shift impacts microbiota function early in disease progression. Here, we analyzed the transition from health to gingivitis through both 16S v4-v5 rRNA amplicon and metatranscriptome sequencing of subgingival plaque samples from individuals undergoing an experimental gingivitis treatment. Beta-diversity analysis of 16S rRNA reveals that samples cluster based on disease severity and patient but not by oral hygiene status. Significant shifts in the abundance of several genera occurred during disease transition, suggesting a dysbiosis due to development of gingivitis. Comparing taxonomic abundance with transcriptomic activity revealed concordance of bacterial diversity composition between the two quantification assays in samples originating from both healthy and diseased teeth. Metatranscriptome sequencing analysis indicates that during the early stages of transition to gingivitis, a number of virulence-related transcripts were significantly differentially expressed in individual and across pooled patient samples. Upregulated genes include those involved in proteolytic and nucleolytic processes, while expression levels of those involved in surface structure assembly and other general virulence functions leading to colonization or adaptation within the host are more dynamic. These findings help characterize the transition from health to periodontal disease and identify genes associated with early disease. IMPORTANCE Although more than 50% of adults have some form of periodontal disease, there remains a significant gap in our understanding of its underlying cause. We initiated this study in order to better characterize the progression from oral health to disease. We first analyzed changes in the abundances of specific microorganisms in dental plaque collected from teeth during health and gingivitis, the mildest form of periodontal disease. We found that the clinical score of disease and patient from whom the sample originated but not tooth brushing are significantly correlated with microbial community composition. While a number of virulence-related gene transcripts are differentially expressed in gingivitis samples relative to health, not all are increased, suggesting that the overall activity of the microbiota is dynamic during disease transition. Better understanding of which microbes are present and their function during early periodontal disease can potentially lead to more targeted prophylactic approaches to prevent disease progression.Emily M. NowickiRaghav ShroffJacqueline A. SingletonDiane E. RenaudDebra WallaceJulie DruryJolene ZirnheldBrock ColletiAndrew D. EllingtonRichard J. LamontDavid A. ScottMarvin WhiteleyAmerican Society for Microbiologyarticledysbiosisgingivitismetatranscriptomeoral microbiologyperiodontitisMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	dysbiosis gingivitis metatranscriptome oral microbiology periodontitis Microbiology QR1-502
spellingShingle	dysbiosis gingivitis metatranscriptome oral microbiology periodontitis Microbiology QR1-502 Emily M. Nowicki Raghav Shroff Jacqueline A. Singleton Diane E. Renaud Debra Wallace Julie Drury Jolene Zirnheld Brock Colleti Andrew D. Ellington Richard J. Lamont David A. Scott Marvin Whiteley Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
description	ABSTRACT Over half of adults experience gingivitis, a mild yet treatable form of periodontal disease caused by the overgrowth of oral microbes. Left untreated, gingivitis can progress to a more severe and irreversible disease, most commonly chronic periodontitis. While periodontal diseases are associated with a shift in the oral microbiota composition, it remains unclear how this shift impacts microbiota function early in disease progression. Here, we analyzed the transition from health to gingivitis through both 16S v4-v5 rRNA amplicon and metatranscriptome sequencing of subgingival plaque samples from individuals undergoing an experimental gingivitis treatment. Beta-diversity analysis of 16S rRNA reveals that samples cluster based on disease severity and patient but not by oral hygiene status. Significant shifts in the abundance of several genera occurred during disease transition, suggesting a dysbiosis due to development of gingivitis. Comparing taxonomic abundance with transcriptomic activity revealed concordance of bacterial diversity composition between the two quantification assays in samples originating from both healthy and diseased teeth. Metatranscriptome sequencing analysis indicates that during the early stages of transition to gingivitis, a number of virulence-related transcripts were significantly differentially expressed in individual and across pooled patient samples. Upregulated genes include those involved in proteolytic and nucleolytic processes, while expression levels of those involved in surface structure assembly and other general virulence functions leading to colonization or adaptation within the host are more dynamic. These findings help characterize the transition from health to periodontal disease and identify genes associated with early disease. IMPORTANCE Although more than 50% of adults have some form of periodontal disease, there remains a significant gap in our understanding of its underlying cause. We initiated this study in order to better characterize the progression from oral health to disease. We first analyzed changes in the abundances of specific microorganisms in dental plaque collected from teeth during health and gingivitis, the mildest form of periodontal disease. We found that the clinical score of disease and patient from whom the sample originated but not tooth brushing are significantly correlated with microbial community composition. While a number of virulence-related gene transcripts are differentially expressed in gingivitis samples relative to health, not all are increased, suggesting that the overall activity of the microbiota is dynamic during disease transition. Better understanding of which microbes are present and their function during early periodontal disease can potentially lead to more targeted prophylactic approaches to prevent disease progression.
format	article
author	Emily M. Nowicki Raghav Shroff Jacqueline A. Singleton Diane E. Renaud Debra Wallace Julie Drury Jolene Zirnheld Brock Colleti Andrew D. Ellington Richard J. Lamont David A. Scott Marvin Whiteley
author_facet	Emily M. Nowicki Raghav Shroff Jacqueline A. Singleton Diane E. Renaud Debra Wallace Julie Drury Jolene Zirnheld Brock Colleti Andrew D. Ellington Richard J. Lamont David A. Scott Marvin Whiteley
author_sort	Emily M. Nowicki
title	Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
title_short	Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
title_full	Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
title_fullStr	Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
title_full_unstemmed	Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis
title_sort	microbiota and metatranscriptome changes accompanying the onset of gingivitis
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/cd490253441c4376b1cc114f8483fea9
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Microbiota and Metatranscriptome Changes Accompanying the Onset of Gingivitis

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