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Tobacco exposure associated with oral microbiota oxygen utilization in the New York City Health and Nutrition Examination Study

Francesco Beghini, Audrey Renson, Christine P. Zolnik, Ludwig Geistlinger, Mykhaylo Usyk, Thomas U. Moody, Lorna Thorpe, Jennifer B. Dowd, Robert Burk, View ORCID ProfileNicola Segata, Heidi E. Jones, Levi Waldron
doi: https://doi.org/10.1101/470286
Francesco Beghini
aCentre for Integrative Biology, University of Trento, Trento, Italy / Via Sommarive, 9 / 38123, Trento, Italy (, )
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  • For correspondence: francesco.beghini@unitn.it nicola.segata@unitn.it
Audrey Renson
bCity University of New York (CUNY) Graduate School of Public Health and Health Policy / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
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  • For correspondence: audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu
Christine P. Zolnik
cDepartment of Pediatrics, Albert Einstein College of Medicine, Bronx, NY, USA (, , , )
dDepartment of Biology, Long Island University, 1 University Plaza, Brooklyn, NY 11201 ()
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  • For correspondence: christine.zolnik@liu.edu mykhaylo.usyk@einstein.yu.edu tu.moody@gmail.com robert.burk@einstein.yu.edu christine.zolnik@liu.edu
Ludwig Geistlinger
bCity University of New York (CUNY) Graduate School of Public Health and Health Policy / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
eInstitute for Implementation Science in Population Health, City University of New York / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
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  • For correspondence: audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu
Mykhaylo Usyk
dDepartment of Biology, Long Island University, 1 University Plaza, Brooklyn, NY 11201 ()
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  • For correspondence: christine.zolnik@liu.edu
Thomas U. Moody
dDepartment of Biology, Long Island University, 1 University Plaza, Brooklyn, NY 11201 ()
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  • For correspondence: christine.zolnik@liu.edu
Lorna Thorpe
fNew York University School of Medicine, 650 1st Ave, New York, NY 10016 ()
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  • For correspondence: lorna.thorpe@nyumc.org
Jennifer B. Dowd
bCity University of New York (CUNY) Graduate School of Public Health and Health Policy / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
gDepartment of Global Health and Social Medicine, King’s College London, The Strand, London WC2R 2LS, United Kingdom ()
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  • For correspondence: audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu jennifer.dowd@kcl.ac.uk
Robert Burk
dDepartment of Biology, Long Island University, 1 University Plaza, Brooklyn, NY 11201 ()
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  • For correspondence: christine.zolnik@liu.edu
Nicola Segata
aCentre for Integrative Biology, University of Trento, Trento, Italy / Via Sommarive, 9 / 38123, Trento, Italy (, )
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  • ORCID record for Nicola Segata
  • For correspondence: francesco.beghini@unitn.it nicola.segata@unitn.it
Heidi E. Jones
bCity University of New York (CUNY) Graduate School of Public Health and Health Policy / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
eInstitute for Implementation Science in Population Health, City University of New York / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
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  • For correspondence: audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu
Levi Waldron
bCity University of New York (CUNY) Graduate School of Public Health and Health Policy / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
eInstitute for Implementation Science in Population Health, City University of New York / 55 W. 125th St. / New York, NY 10027, United States (, ; ; ; )
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  • For correspondence: audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu audrey.o.renson@gmail.com Ludwig.Geistlinger@sph.cuny.edu Jennifer.Dowd@sph.cuny.edu Heidi.Jones@sph.cuny.edu Levi.Waldron@sph.cuny.edu
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ABSTRACT

Purpose The effect of tobacco exposure on the oral microbiome has not been established.

Methods We performed amplicon sequencing of the 16S ribosomal RNA gene V4 variable region to estimate bacterial community characteristics in 259 oral rinse samples, selected based on self-reported smoking and serum cotinine levels, from the 2013-14 New York City Health and Nutrition Examination Study. We identified differentially abundant operational taxonomic units (OTUs) by primary and secondhand tobacco exposure, and employed “microbe set enrichment analysis” to assess shifts in microbial oxygen utilization.

Results Cigarette smoking was associated with depletion of aerobic OTUs (Enrichment Score test statistic ES = -0.75, p = 0.002) with a minority (29%) of aerobic OTUs enriched in current smokers compared to never smokers. Consistent shifts in the microbiota were observed for current cigarette smokers as for non-smokers with secondhand exposure as measured by serum cotinine levels. Differential abundance findings were similar in crude and adjusted analyses.

Conclusion Results support a plausible link between tobacco exposure and shifts in the oral microbiome at the population level through three lines of evidence: 1) a shift in microbiota oxygen utilization associated with primary tobacco smoke exposure, 2) consistency of abundance fold-changes associated with current smoking and shifts along the gradient of secondhand smoke exposure among non-smokers, and 3) consistency after adjusting for a priori hypothesized confounders.

  • Cigarette smoke was associated with microbial anaerobiosis in oral rinse specimens

  • The microbiome shifts associated with smoking and secondhand exposure were correlated

  • Shifts in oral bacterial oxygen utilization may mediate smoking and health outcomes

  • We propose “microbe set enrichment analysis” for interpreting shifts in the microbiome

List of abbreviations
CI
Confidence Interval
CUNY
City University of New York
DNA
Deoxyribonucleic Acid
ES
Enrichment Score
FDR
False Discovery Rate
GSEA
Gene Set Enrichment Analysis
GSVA
Gene Set Variation Analysis
HMP
Human MIcrobiome Project
IRB
Institutional Review Board
NHANES
National Health Nutrition and Examination Survey
NYC DOHMH
New York City Department of Health and Mental Hygiene
NYC HANES
New York City Health Nutrition and Examination Survey
OR
Odds Ratio
ORA
Over-representation Analysis
OTU
Operational Taxonomic Unit
PCOA
Principal Coordinates Analysis
PERMANOVA
Permutational Multivariate Analysis of Variance
RNA
Ribonucleic Acid
rRNA
Ribosomal Ribonucleic Acid
Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 14, 2018.
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Tobacco exposure associated with oral microbiota oxygen utilization in the New York City Health and Nutrition Examination Study
Francesco Beghini, Audrey Renson, Christine P. Zolnik, Ludwig Geistlinger, Mykhaylo Usyk, Thomas U. Moody, Lorna Thorpe, Jennifer B. Dowd, Robert Burk, Nicola Segata, Heidi E. Jones, Levi Waldron
bioRxiv 470286; doi: https://doi.org/10.1101/470286
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Tobacco exposure associated with oral microbiota oxygen utilization in the New York City Health and Nutrition Examination Study
Francesco Beghini, Audrey Renson, Christine P. Zolnik, Ludwig Geistlinger, Mykhaylo Usyk, Thomas U. Moody, Lorna Thorpe, Jennifer B. Dowd, Robert Burk, Nicola Segata, Heidi E. Jones, Levi Waldron
bioRxiv 470286; doi: https://doi.org/10.1101/470286

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