Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins

BackgroundStaphylococcus aureus is a gram-positive bacterium commonly found in the nares and oropharynx of one in three individuals and has the potential to cause significant health problems. With antibiotic-resistant strains causing 11,000 deaths yearly and ~2% of the population nasally colonized w...

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Main Authors: Mark R. Dalman, W. Brian Simison, Danny Nielsen, Sabana Bhatta, Noor Ramahi, Clair Yee, Dipendra Thapaliya, Jhalka Kadariya, Shanice Cheatham, Hailee Olson, Tara C. Smith
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiomes
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Online Access:https://www.frontiersin.org/articles/10.3389/frmbi.2024.1457940/full
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author Mark R. Dalman
W. Brian Simison
Danny Nielsen
Sabana Bhatta
Noor Ramahi
Clair Yee
Dipendra Thapaliya
Jhalka Kadariya
Shanice Cheatham
Hailee Olson
Tara C. Smith
author_facet Mark R. Dalman
W. Brian Simison
Danny Nielsen
Sabana Bhatta
Noor Ramahi
Clair Yee
Dipendra Thapaliya
Jhalka Kadariya
Shanice Cheatham
Hailee Olson
Tara C. Smith
author_sort Mark R. Dalman
collection DOAJ
description BackgroundStaphylococcus aureus is a gram-positive bacterium commonly found in the nares and oropharynx of one in three individuals and has the potential to cause significant health problems. With antibiotic-resistant strains causing 11,000 deaths yearly and ~2% of the population nasally colonized with methicillin-resistant S. aureus, a search for predictive markers and associative relationships between carriage have been long-sought goals. Within our study, we leveraged monozygotic twin participants in concert with multi-site microbiome analyses to characterize the impacts of S. aureus on composition.ResultsWe recruited 147 monozygotic twin pairs and characterized three sites, i.e., the nares, oropharynx, and hand microbiomes, using 16S rRNA v3-v4 sequencing in addition to S. aureus carriage status. The prevalence of S. aureus was highest in the oropharynx followed by nares and hand with concordance between twin pairs highest in the nares, followed by oropharynx. The detection of S. aureus was statistically correlated with differences in microbiome composition across sites, as indicated by beta diversity and DESeq2 analyses. Microbiome composition was most similar in twins’ nares that were S. aureus culture-positive concordant, whereas twins that were culture-negative concordant had the most similarity in the oropharynx. Of significance, Moraxella nonliquefacians and Capnocytophaga were inversely associated with S. aureus in the nares and oropharynx, respectively.ConclusionsThis improved understanding of S. aureus colonization in nares, oropharynx, and hand microbiomes in monozygotic twin pairs is a further step towards unraveling the degree to which the microbiome is influenced by host genetics and S. aureus carriage.
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spelling doaj-art-7e35438fe51d49f09fe9ed5e97f0b3352025-01-20T07:20:29ZengFrontiers Media S.A.Frontiers in Microbiomes2813-43382025-01-01310.3389/frmbi.2024.14579401457940Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twinsMark R. Dalman0W. Brian Simison1Danny Nielsen2Sabana Bhatta3Noor Ramahi4Clair Yee5Dipendra Thapaliya6Jhalka Kadariya7Shanice Cheatham8Hailee Olson9Tara C. Smith10College of Podiatric Medicine, Kent State University, Kent, OH, United StatesCenter for Comparative Genomics, California Academy of Sciences, San Francisco, CA, United StatesDepartment of Natural Resources and Environmental Science, University of Nevada, Reno, Reno, NV, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesCollege of Public Health, Kent State University, Kent, OH, United StatesBackgroundStaphylococcus aureus is a gram-positive bacterium commonly found in the nares and oropharynx of one in three individuals and has the potential to cause significant health problems. With antibiotic-resistant strains causing 11,000 deaths yearly and ~2% of the population nasally colonized with methicillin-resistant S. aureus, a search for predictive markers and associative relationships between carriage have been long-sought goals. Within our study, we leveraged monozygotic twin participants in concert with multi-site microbiome analyses to characterize the impacts of S. aureus on composition.ResultsWe recruited 147 monozygotic twin pairs and characterized three sites, i.e., the nares, oropharynx, and hand microbiomes, using 16S rRNA v3-v4 sequencing in addition to S. aureus carriage status. The prevalence of S. aureus was highest in the oropharynx followed by nares and hand with concordance between twin pairs highest in the nares, followed by oropharynx. The detection of S. aureus was statistically correlated with differences in microbiome composition across sites, as indicated by beta diversity and DESeq2 analyses. Microbiome composition was most similar in twins’ nares that were S. aureus culture-positive concordant, whereas twins that were culture-negative concordant had the most similarity in the oropharynx. Of significance, Moraxella nonliquefacians and Capnocytophaga were inversely associated with S. aureus in the nares and oropharynx, respectively.ConclusionsThis improved understanding of S. aureus colonization in nares, oropharynx, and hand microbiomes in monozygotic twin pairs is a further step towards unraveling the degree to which the microbiome is influenced by host genetics and S. aureus carriage.https://www.frontiersin.org/articles/10.3389/frmbi.2024.1457940/fullmicrobiome16S rRNAStaphylococcus aureusmonozygotic twinsnaresoropharynx
spellingShingle Mark R. Dalman
W. Brian Simison
Danny Nielsen
Sabana Bhatta
Noor Ramahi
Clair Yee
Dipendra Thapaliya
Jhalka Kadariya
Shanice Cheatham
Hailee Olson
Tara C. Smith
Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins
Frontiers in Microbiomes
microbiome
16S rRNA
Staphylococcus aureus
monozygotic twins
nares
oropharynx
title Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins
title_full Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins
title_fullStr Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins
title_full_unstemmed Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins
title_short Staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx, not the hand, of monozygotic twins
title_sort staphylococcus aureus carriage is associated with microbiome composition in the nares and oropharynx not the hand of monozygotic twins
topic microbiome
16S rRNA
Staphylococcus aureus
monozygotic twins
nares
oropharynx
url https://www.frontiersin.org/articles/10.3389/frmbi.2024.1457940/full
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