Disordered microbial communities in the upper respiratory tract of cigarette smokers
Cigarette smokers have an increased risk of infectious diseases involving the respiratory tract. Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-...
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description | Cigarette smokers have an increased risk of infectious diseases involving the respiratory tract. Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-independent high-density sequencing to analyze the microbiota from the right and left nasopharynx and oropharynx of 29 smoking and 33 nonsmoking healthy asymptomatic adults to assess microbial composition and effects of cigarette smoking. Bacterial communities were profiled using 454 pyrosequencing of 16S sequence tags (803,391 total reads), aligned to 16S rRNA databases, and communities compared using the UniFrac distance metric. A Random Forest machine-learning algorithm was used to predict smoking status and identify taxa that best distinguished between smokers and nonsmokers. Community composition was primarily determined by airway site, with individuals exhibiting minimal side-of-body or temporal variation. Within airway habitats, microbiota from smokers were significantly more diverse than nonsmokers and clustered separately. The distributions of several genera were systematically altered by smoking in both the oro- and nasopharynx, and there was an enrichment of anaerobic lineages associated with periodontal disease in the oropharynx. These results indicate that distinct regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population. |
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Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-independent high-density sequencing to analyze the microbiota from the right and left nasopharynx and oropharynx of 29 smoking and 33 nonsmoking healthy asymptomatic adults to assess microbial composition and effects of cigarette smoking. Bacterial communities were profiled using 454 pyrosequencing of 16S sequence tags (803,391 total reads), aligned to 16S rRNA databases, and communities compared using the UniFrac distance metric. A Random Forest machine-learning algorithm was used to predict smoking status and identify taxa that best distinguished between smokers and nonsmokers. Community composition was primarily determined by airway site, with individuals exhibiting minimal side-of-body or temporal variation. Within airway habitats, microbiota from smokers were significantly more diverse than nonsmokers and clustered separately. The distributions of several genera were systematically altered by smoking in both the oro- and nasopharynx, and there was an enrichment of anaerobic lineages associated with periodontal disease in the oropharynx. These results indicate that distinct regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0015216</identifier><identifier>PMID: 21188149</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Adults ; Algorithms ; Artificial Intelligence ; Bacteria ; Bacterial Typing Techniques ; Bioinformatics ; Biology ; Cigarette smoking ; Cigarettes ; Communicable diseases ; Communities ; Community composition ; Comparative analysis ; Complications ; Composition effects ; Critical care ; DNA, Bacterial - genetics ; Epidemiology ; Female ; Gram-positive bacteria ; Health risks ; Humans ; Infectious diseases ; Klebsiella ; Learning algorithms ; Machine learning ; Magnetics ; Male ; Medicine ; Microbial activity ; Microbiomes ; Microbiota ; Microbiota (Symbiotic organisms) ; Microorganisms ; Middle Aged ; Multiculturalism & pluralism ; Nasopharynx ; Oropharynx ; Pathogenesis ; Periodontal disease ; Periodontics ; Polymerase Chain Reaction - methods ; Pseudomonas aeruginosa ; Respiration ; Respiratory System - microbiology ; Respiratory tract ; Respiratory tract diseases ; RNA ; RNA, Ribosomal, 16S - metabolism ; rRNA 16S ; Sequence Analysis, DNA - methods ; Smokers ; Smoking ; Smoking - adverse effects ; Streptococcus infections ; Studies ; Taxa ; Temporal variations</subject><ispartof>PloS one, 2010-12, Vol.5 (12), p.e15216-e15216</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Charlson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Charlson et al. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c757t-6041d79c277b185e3ea306a1a10b90b28449e99e63d8817364b246d208bacd3c3</citedby><cites>FETCH-LOGICAL-c757t-6041d79c277b185e3ea306a1a10b90b28449e99e63d8817364b246d208bacd3c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3004851/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3004851/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21188149$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Charlson, Emily S</creatorcontrib><creatorcontrib>Chen, Jun</creatorcontrib><creatorcontrib>Custers-Allen, Rebecca</creatorcontrib><creatorcontrib>Bittinger, Kyle</creatorcontrib><creatorcontrib>Li, Hongzhe</creatorcontrib><creatorcontrib>Sinha, Rohini</creatorcontrib><creatorcontrib>Hwang, Jennifer</creatorcontrib><creatorcontrib>Bushman, Frederic D</creatorcontrib><creatorcontrib>Collman, Ronald G</creatorcontrib><title>Disordered microbial communities in the upper respiratory tract of cigarette smokers</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Cigarette smokers have an increased risk of infectious diseases involving the respiratory tract. Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-independent high-density sequencing to analyze the microbiota from the right and left nasopharynx and oropharynx of 29 smoking and 33 nonsmoking healthy asymptomatic adults to assess microbial composition and effects of cigarette smoking. Bacterial communities were profiled using 454 pyrosequencing of 16S sequence tags (803,391 total reads), aligned to 16S rRNA databases, and communities compared using the UniFrac distance metric. A Random Forest machine-learning algorithm was used to predict smoking status and identify taxa that best distinguished between smokers and nonsmokers. Community composition was primarily determined by airway site, with individuals exhibiting minimal side-of-body or temporal variation. 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These results indicate that distinct regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population.</description><subject>Adult</subject><subject>Adults</subject><subject>Algorithms</subject><subject>Artificial Intelligence</subject><subject>Bacteria</subject><subject>Bacterial Typing Techniques</subject><subject>Bioinformatics</subject><subject>Biology</subject><subject>Cigarette smoking</subject><subject>Cigarettes</subject><subject>Communicable diseases</subject><subject>Communities</subject><subject>Community composition</subject><subject>Comparative analysis</subject><subject>Complications</subject><subject>Composition effects</subject><subject>Critical care</subject><subject>DNA, Bacterial - genetics</subject><subject>Epidemiology</subject><subject>Female</subject><subject>Gram-positive bacteria</subject><subject>Health risks</subject><subject>Humans</subject><subject>Infectious diseases</subject><subject>Klebsiella</subject><subject>Learning algorithms</subject><subject>Machine learning</subject><subject>Magnetics</subject><subject>Male</subject><subject>Medicine</subject><subject>Microbial activity</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Middle Aged</subject><subject>Multiculturalism & pluralism</subject><subject>Nasopharynx</subject><subject>Oropharynx</subject><subject>Pathogenesis</subject><subject>Periodontal disease</subject><subject>Periodontics</subject><subject>Polymerase Chain Reaction - 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genetics</topic><topic>Epidemiology</topic><topic>Female</topic><topic>Gram-positive bacteria</topic><topic>Health risks</topic><topic>Humans</topic><topic>Infectious diseases</topic><topic>Klebsiella</topic><topic>Learning algorithms</topic><topic>Machine learning</topic><topic>Magnetics</topic><topic>Male</topic><topic>Medicine</topic><topic>Microbial activity</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Microbiota (Symbiotic organisms)</topic><topic>Microorganisms</topic><topic>Middle Aged</topic><topic>Multiculturalism & pluralism</topic><topic>Nasopharynx</topic><topic>Oropharynx</topic><topic>Pathogenesis</topic><topic>Periodontal disease</topic><topic>Periodontics</topic><topic>Polymerase Chain Reaction - methods</topic><topic>Pseudomonas aeruginosa</topic><topic>Respiration</topic><topic>Respiratory System - microbiology</topic><topic>Respiratory tract</topic><topic>Respiratory tract diseases</topic><topic>RNA</topic><topic>RNA, Ribosomal, 16S - metabolism</topic><topic>rRNA 16S</topic><topic>Sequence Analysis, DNA - 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Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-independent high-density sequencing to analyze the microbiota from the right and left nasopharynx and oropharynx of 29 smoking and 33 nonsmoking healthy asymptomatic adults to assess microbial composition and effects of cigarette smoking. Bacterial communities were profiled using 454 pyrosequencing of 16S sequence tags (803,391 total reads), aligned to 16S rRNA databases, and communities compared using the UniFrac distance metric. A Random Forest machine-learning algorithm was used to predict smoking status and identify taxa that best distinguished between smokers and nonsmokers. Community composition was primarily determined by airway site, with individuals exhibiting minimal side-of-body or temporal variation. Within airway habitats, microbiota from smokers were significantly more diverse than nonsmokers and clustered separately. The distributions of several genera were systematically altered by smoking in both the oro- and nasopharynx, and there was an enrichment of anaerobic lineages associated with periodontal disease in the oropharynx. These results indicate that distinct regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21188149</pmid><doi>10.1371/journal.pone.0015216</doi><tpages>e15216</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adult Adults Algorithms Artificial Intelligence Bacteria Bacterial Typing Techniques Bioinformatics Biology Cigarette smoking Cigarettes Communicable diseases Communities Community composition Comparative analysis Complications Composition effects Critical care DNA, Bacterial - genetics Epidemiology Female Gram-positive bacteria Health risks Humans Infectious diseases Klebsiella Learning algorithms Machine learning Magnetics Male Medicine Microbial activity Microbiomes Microbiota Microbiota (Symbiotic organisms) Microorganisms Middle Aged Multiculturalism & pluralism Nasopharynx Oropharynx Pathogenesis Periodontal disease Periodontics Polymerase Chain Reaction - methods Pseudomonas aeruginosa Respiration Respiratory System - microbiology Respiratory tract Respiratory tract diseases RNA RNA, Ribosomal, 16S - metabolism rRNA 16S Sequence Analysis, DNA - methods Smokers Smoking Smoking - adverse effects Streptococcus infections Studies Taxa Temporal variations |
title | Disordered microbial communities in the upper respiratory tract of cigarette smokers |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-04T17%3A56%3A17IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Disordered%20microbial%20communities%20in%20the%20upper%20respiratory%20tract%20of%20cigarette%20smokers&rft.jtitle=PloS%20one&rft.au=Charlson,%20Emily%20S&rft.date=2010-12-20&rft.volume=5&rft.issue=12&rft.spage=e15216&rft.epage=e15216&rft.pages=e15216-e15216&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0015216&rft_dat=%3Cgale_plos_%3EA473814375%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1312181233&rft_id=info:pmid/21188149&rft_galeid=A473814375&rft_doaj_id=oai_doaj_org_article_60b548db5f2b4997928863e3614337dc&rfr_iscdi=true |