Cigarette smoking and the oral microbiome in a large study of American adults

Jing Wu, Brandilyn A. Peters, Christine Dominianni, Yilong Zhang, Zhiheng Pei, Liying Yang, Yingfei Ma, Mark P. Purdue, Eric J. Jacobs, Susan M. Gapstur, Huilin Li, Alexander V. Alekseyenko, Richard B. Hayes, Jiyoung Ahn

Research output: Contribution to journalArticle

100 Citations (Scopus)

Abstract

Oral microbiome dysbiosis is associated with oral disease and potentially with systemic diseases; however, the determinants of these microbial imbalances are largely unknown. In a study of 1204 US adults, we assessed the relationship of cigarette smoking with the oral microbiome. 16S rRNA gene sequencing was performed on DNA from oral wash samples, sequences were clustered into operational taxonomic units (OTUs) using QIIME and metagenomic content was inferred using PICRUSt. Overall oral microbiome composition differed between current and non-current (former and never) smokers (P<0.001). Current smokers had lower relative abundance of the phylum Proteobacteria (4.6%) compared with never smokers (11.7%) (false discovery rate q=5.2 × 10 -7), with no difference between former and never smokers; the depletion of Proteobacteria in current smokers was also observed at class, genus and OTU levels. Taxa not belonging to Proteobacteria were also associated with smoking: the genera Capnocytophaga, Peptostreptococcus and Leptotrichia were depleted, while Atopobium and Streptococcus were enriched, in current compared with never smokers. Functional analysis from inferred metagenomes showed that bacterial genera depleted by smoking were related to carbohydrate and energy metabolism, and to xenobiotic metabolism. Our findings demonstrate that smoking alters the oral microbiome, potentially leading to shifts in functional pathways with implications for smoking-related diseases.

Original languageEnglish (US)
Pages (from-to)2435-2446
Number of pages12
JournalISME Journal
Volume10
Issue number10
DOIs
StatePublished - Oct 1 2016
Externally publishedYes

Fingerprint

smoking (habit)
Microbiota
smoking
mouth
Proteobacteria
Smoking
Capnocytophaga
Atopobium
Leptotrichia
Mouth Diseases
Peptostreptococcus
metabolism
Dysbiosis
Metagenome
mouth diseases
Metagenomics
Streptococcus
Carbohydrate Metabolism
Xenobiotics
xenobiotics

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Wu, J., Peters, B. A., Dominianni, C., Zhang, Y., Pei, Z., Yang, L., ... Ahn, J. (2016). Cigarette smoking and the oral microbiome in a large study of American adults. ISME Journal, 10(10), 2435-2446. https://doi.org/10.1038/ismej.2016.37

Cigarette smoking and the oral microbiome in a large study of American adults. / Wu, Jing; Peters, Brandilyn A.; Dominianni, Christine; Zhang, Yilong; Pei, Zhiheng; Yang, Liying; Ma, Yingfei; Purdue, Mark P.; Jacobs, Eric J.; Gapstur, Susan M.; Li, Huilin; Alekseyenko, Alexander V.; Hayes, Richard B.; Ahn, Jiyoung.

In: ISME Journal, Vol. 10, No. 10, 01.10.2016, p. 2435-2446.

Research output: Contribution to journalArticle

Wu, J, Peters, BA, Dominianni, C, Zhang, Y, Pei, Z, Yang, L, Ma, Y, Purdue, MP, Jacobs, EJ, Gapstur, SM, Li, H, Alekseyenko, AV, Hayes, RB & Ahn, J 2016, 'Cigarette smoking and the oral microbiome in a large study of American adults', ISME Journal, vol. 10, no. 10, pp. 2435-2446. https://doi.org/10.1038/ismej.2016.37
Wu, Jing ; Peters, Brandilyn A. ; Dominianni, Christine ; Zhang, Yilong ; Pei, Zhiheng ; Yang, Liying ; Ma, Yingfei ; Purdue, Mark P. ; Jacobs, Eric J. ; Gapstur, Susan M. ; Li, Huilin ; Alekseyenko, Alexander V. ; Hayes, Richard B. ; Ahn, Jiyoung. / Cigarette smoking and the oral microbiome in a large study of American adults. In: ISME Journal. 2016 ; Vol. 10, No. 10. pp. 2435-2446.
@article{1854fe73a5f64c39be14684238d803b5,
title = "Cigarette smoking and the oral microbiome in a large study of American adults",
abstract = "Oral microbiome dysbiosis is associated with oral disease and potentially with systemic diseases; however, the determinants of these microbial imbalances are largely unknown. In a study of 1204 US adults, we assessed the relationship of cigarette smoking with the oral microbiome. 16S rRNA gene sequencing was performed on DNA from oral wash samples, sequences were clustered into operational taxonomic units (OTUs) using QIIME and metagenomic content was inferred using PICRUSt. Overall oral microbiome composition differed between current and non-current (former and never) smokers (P<0.001). Current smokers had lower relative abundance of the phylum Proteobacteria (4.6{\%}) compared with never smokers (11.7{\%}) (false discovery rate q=5.2 × 10 -7), with no difference between former and never smokers; the depletion of Proteobacteria in current smokers was also observed at class, genus and OTU levels. Taxa not belonging to Proteobacteria were also associated with smoking: the genera Capnocytophaga, Peptostreptococcus and Leptotrichia were depleted, while Atopobium and Streptococcus were enriched, in current compared with never smokers. Functional analysis from inferred metagenomes showed that bacterial genera depleted by smoking were related to carbohydrate and energy metabolism, and to xenobiotic metabolism. Our findings demonstrate that smoking alters the oral microbiome, potentially leading to shifts in functional pathways with implications for smoking-related diseases.",
author = "Jing Wu and Peters, {Brandilyn A.} and Christine Dominianni and Yilong Zhang and Zhiheng Pei and Liying Yang and Yingfei Ma and Purdue, {Mark P.} and Jacobs, {Eric J.} and Gapstur, {Susan M.} and Huilin Li and Alekseyenko, {Alexander V.} and Hayes, {Richard B.} and Jiyoung Ahn",
year = "2016",
month = "10",
day = "1",
doi = "10.1038/ismej.2016.37",
language = "English (US)",
volume = "10",
pages = "2435--2446",
journal = "ISME Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",
number = "10",

}

TY - JOUR

T1 - Cigarette smoking and the oral microbiome in a large study of American adults

AU - Wu, Jing

AU - Peters, Brandilyn A.

AU - Dominianni, Christine

AU - Zhang, Yilong

AU - Pei, Zhiheng

AU - Yang, Liying

AU - Ma, Yingfei

AU - Purdue, Mark P.

AU - Jacobs, Eric J.

AU - Gapstur, Susan M.

AU - Li, Huilin

AU - Alekseyenko, Alexander V.

AU - Hayes, Richard B.

AU - Ahn, Jiyoung

PY - 2016/10/1

Y1 - 2016/10/1

N2 - Oral microbiome dysbiosis is associated with oral disease and potentially with systemic diseases; however, the determinants of these microbial imbalances are largely unknown. In a study of 1204 US adults, we assessed the relationship of cigarette smoking with the oral microbiome. 16S rRNA gene sequencing was performed on DNA from oral wash samples, sequences were clustered into operational taxonomic units (OTUs) using QIIME and metagenomic content was inferred using PICRUSt. Overall oral microbiome composition differed between current and non-current (former and never) smokers (P<0.001). Current smokers had lower relative abundance of the phylum Proteobacteria (4.6%) compared with never smokers (11.7%) (false discovery rate q=5.2 × 10 -7), with no difference between former and never smokers; the depletion of Proteobacteria in current smokers was also observed at class, genus and OTU levels. Taxa not belonging to Proteobacteria were also associated with smoking: the genera Capnocytophaga, Peptostreptococcus and Leptotrichia were depleted, while Atopobium and Streptococcus were enriched, in current compared with never smokers. Functional analysis from inferred metagenomes showed that bacterial genera depleted by smoking were related to carbohydrate and energy metabolism, and to xenobiotic metabolism. Our findings demonstrate that smoking alters the oral microbiome, potentially leading to shifts in functional pathways with implications for smoking-related diseases.

AB - Oral microbiome dysbiosis is associated with oral disease and potentially with systemic diseases; however, the determinants of these microbial imbalances are largely unknown. In a study of 1204 US adults, we assessed the relationship of cigarette smoking with the oral microbiome. 16S rRNA gene sequencing was performed on DNA from oral wash samples, sequences were clustered into operational taxonomic units (OTUs) using QIIME and metagenomic content was inferred using PICRUSt. Overall oral microbiome composition differed between current and non-current (former and never) smokers (P<0.001). Current smokers had lower relative abundance of the phylum Proteobacteria (4.6%) compared with never smokers (11.7%) (false discovery rate q=5.2 × 10 -7), with no difference between former and never smokers; the depletion of Proteobacteria in current smokers was also observed at class, genus and OTU levels. Taxa not belonging to Proteobacteria were also associated with smoking: the genera Capnocytophaga, Peptostreptococcus and Leptotrichia were depleted, while Atopobium and Streptococcus were enriched, in current compared with never smokers. Functional analysis from inferred metagenomes showed that bacterial genera depleted by smoking were related to carbohydrate and energy metabolism, and to xenobiotic metabolism. Our findings demonstrate that smoking alters the oral microbiome, potentially leading to shifts in functional pathways with implications for smoking-related diseases.

UR - http://www.scopus.com/inward/record.url?scp=84961730132&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84961730132&partnerID=8YFLogxK

U2 - 10.1038/ismej.2016.37

DO - 10.1038/ismej.2016.37

M3 - Article

C2 - 27015003

AN - SCOPUS:84961730132

VL - 10

SP - 2435

EP - 2446

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 10

ER -