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Compositional profile of mucosal bacteriome of smokers and smokeless tobacco users

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Abstract

Introduction

Smoked, and especially smokeless, tobacco are major causes of oral cancer globally. Here, we examine the oral bacteriome of smokers and of smokeless tobacco users, in comparison to healthy controls, using 16S rRNA gene sequencing.

Methods

Oral swab samples were collected from smokers, smokeless tobacco users, and healthy controls (n = 44). Microbial DNA was extracted and the 16S rRNA gene profiled using the Illumina MiSeq platform. Sequencing reads were processed using DADA2, and taxonomical classification was performed using the phylogenetic placement method. Differentially abundant taxa were identified using DESeq2, while functional metagenomes based on KEGG orthology abundance were inferred using LIMMA.

Results

A significantly higher microbial diversity was observed in smokeless tobacco users and smokers relative to controls (P < 0.05). Compositional differences in microbial communities were observed in all comparisons with healthy controls (PERMANOVA P < 0.05) but not between smokers and smokeless tobacco users. Levels of Fusobacterium spp., Saccharibacterium spp., and members of Shuttleworthia were elevated in smokers when compared to controls (BH adj P < 0.01). In addition, the relative abundance of three bacterial taxa belonging to genera Fusobacterium spp., Catonella, and Fretibacterium spp. was significantly increased in smokeless tobacco users relative to controls (BH adj P < 0.01). Major functional pathways significantly increased in smokeless tobacco users relative to both controls, and smokers were similar and involved amino acid metabolism including glutamate and aspartate biosynthesis and degradation (log FC > 1.5; BH adj P < 0.01).

Conclusions

A distinct taxonomic and functional profile of oral microbiome in smokers and smokeless tobacco users as compared to healthy controls implicates a significant role of microbes and their metabolites in diseases associated with tobacco use including oral cancer.

Clinical relevance

Future efforts in preventive, diagnostic, curative, and prognostic strategies for diseases associated with tobacco use in smokers and smokeless tobacco users could incorporate the oral microbiome.

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Author information

Authors and Affiliations

  1. Faculty of Dentistry, University of Hong Kong, Prince Philip Dental Hospital, Street 34 Hospital Rd, Sai Ying Pun, Hong Kong, SAR, China

    Divya Gopinath, Michael George Botelho & Newell W. Johnson

  2. Clinical Oral Health Sciences, School of Dentistry, International Medical University, Kuala , Lumpur, Malaysia

    Divya Gopinath

  3. School of Pharmacy, Monash University Malaysia, Subang Jaya, Malaysia

    Chong Chun Wie

  4. Human Molecular Genetics Lab, Rajiv Gandhi Centre for Biotechnology, Trivandrum, India

    Moinak Banerjee

  5. Saveetha Dental College and Hospital, Saveetha University, Chennai, India

    Lakshmi Thangavelu , Pradeep Kumar R & Deepak Nallaswamy

  6. Menzies Health Institute Queensland and School of Dentistry and Oral Health, Griffith University, Southport, QLD, Australia

    Newell W. Johnson

  7. Faculty of Dentistry, Oral and Craniofacial Sciences, King’s College London, London, UK

    Newell W. Johnson

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  1. Divya Gopinath
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  8. Newell W. Johnson
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Contributions

DVG contributed to conception, design, data acquisition and interpretation, and statistical analysis and drafted and critically revised the manuscript. CCW performed the statistical analysis. MB contributed to design and data acquisition and interpretation. LT, PK, and DN contributed to design and data acquisition and interpretation. MGB contributed to the conception and design and critically revised the manuscript. NWJ contributed to the conception and design and critically revised the manuscript. All authors gave their final approval.

Corresponding authors

Correspondence to Michael George Botelho or Newell W. Johnson.

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The authors declare no competing interests.

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Gopinath, D., Wie, C.C., Banerjee, M. et al. Compositional profile of mucosal bacteriome of smokers and smokeless tobacco users. Clin Oral Invest 26, 1647–1656 (2022). https://doi.org/10.1007/s00784-021-04137-7

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  • DOI: https://doi.org/10.1007/s00784-021-04137-7

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