Journal article
The making of a miscreant: tobacco smoke and the creation of pathogen-rich biofilms
NPJ biofilms and microbiomes, Vol.3(1), pp.26-9
10/24/2017
DOI: 10.1038/s41522-017-0033-2
PMCID: PMC5655325
PMID: 29081982
Abstract
We have previously reported that oral biofilms in clinically healthy smokers are pathogen-rich, and that this enrichment occurs within 24 h of biofilm formation. The present investigation aimed to identify a mechanism by which smoking creates this altered community structure. By combining in vitro microbial-mucosal interface models of commensal (consisting of Streptococcus oralis, Streptococcus sanguis, Streptococcus mitis, Actinomyces naeslundii, Neisseria mucosa and Veillonella parvula) and pathogen-rich (comprising S. oralis, S. sanguis, S. mitis, A. naeslundii, N. mucosa and V. parvula, Fusobacterium nucleatum, Porphyromonas gingivalis, Filifactor alocis, Dialister pneumosintes, Selenonomas sputigena, Selenominas noxia, Catonella morbi, Parvimonas micra and Tannerella forsythia) communities with metatranscriptomics, targeted proteomics and fluorescent microscopy, we demonstrate that smoke exposure significantly downregulates essential metabolic functions within commensal biofilms, while significantly increasing expression of virulence genes, notably lipopolysaccharide (LPS), flagella and capsule synthesis. By contrast, in pathogen-rich biofilms several metabolic pathways were over-expressed in response to smoke exposure. Under smoke-rich conditions, epithelial cells mounted an early and amplified pro-inflammatory and oxidative stress response to these virulence-enhanced commensal biofilms, and a muted early response to pathogen-rich biofilms. Commensal biofilms also demonstrated early and widespread cell death. Similar results were observed when smoke-free epithelial cells were challenged with smoke-conditioned biofilms, but not vice versa. In conclusion, our data suggest that smoke-induced transcriptional shifts in commensal biofilms triggers a florid pro-inflammatory response, leading to early commensal death, which may preclude niche saturation by these beneficial organisms. The cytokine-rich, pro-oxidant, anaerobic environment sustains inflammophilic bacteria, and, in the absence of commensal antagonism, may promote the creation of pathogen-rich biofilms in smokers.
Details
- Title: Subtitle
- The making of a miscreant: tobacco smoke and the creation of pathogen-rich biofilms
- Creators
- Samir A. Shah - The Ohio State UniversitySukirth M. Ganesan - The Ohio State UniversitySaradhadevi Varadharaj - The Ohio State UniversityShareef M. Dabdoub - The Ohio State UniversityJohn D. Walters - The Ohio State UniversityPurnima S. Kumar - The Ohio State University
- Resource Type
- Journal article
- Publication Details
- NPJ biofilms and microbiomes, Vol.3(1), pp.26-9
- DOI
- 10.1038/s41522-017-0033-2
- PMID
- 29081982
- PMCID
- PMC5655325
- NLM abbreviation
- NPJ Biofilms Microbiomes
- ISSN
- 2055-5008
- eISSN
- 2055-5008
- Publisher
- Springer Nature
- Number of pages
- 9
- Grant note
- P30CA016058 / NATIONAL CANCER INSTITUTE; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA; NIH National Cancer Institute (NCI) R01DE022579 / NATIONAL INSTITUTE OF DENTAL & CRANIOFACIAL RESEARCH; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA; NIH National Institute of Dental & Craniofacial Research (NIDCR) R01 DE022579 / NIDCR grant
- Language
- English
- Date published
- 10/24/2017
- Academic Unit
- Dental Research; Periodontics
- Record Identifier
- 9984367640302771
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