Genomic attributes of airway commensal bacteria and mucosa

Abstract Microbial communities at the airway mucosal barrier are conserved and highly ordered, in likelihood reflecting co-evolution with human host factors. Freed of selection to digest nutrients, the airway microbiome underpins cognate management of mucosal immunity and pathogen resistance. We sho...

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Main Authors: Leah Cuthbertson, Ulrike Löber, Jonathan S. Ish-Horowicz, Claire N. McBrien, Colin Churchward, Jeremy C. Parker, Michael T. Olanipekun, Conor Burke, Aisling McGowan, Gwyneth A. Davies, Keir E. Lewis, Julian M. Hopkin, Kian Fan Chung, Orla O’Carroll, John Faul, Joy Creaser-Thomas, Mark Andrews, Robin Ghosal, Stefan Piatek, Saffron A. G. Willis-Owen, Theda U. P. Bartolomaeus, Till Birkner, Sarah Dwyer, Nitin Kumar, Elena M. Turek, A. William Musk, Jennie Hui, Michael Hunter, Alan James, Marc-Emmanuel Dumas, Sarah Filippi, Michael J. Cox, Trevor D. Lawley, Sofia K. Forslund, Miriam F. Moffatt, William. O. C. Cookson
Format: Article
Language:English
Published: Nature Portfolio 2024-02-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-05840-3
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author Leah Cuthbertson
Ulrike Löber
Jonathan S. Ish-Horowicz
Claire N. McBrien
Colin Churchward
Jeremy C. Parker
Michael T. Olanipekun
Conor Burke
Aisling McGowan
Gwyneth A. Davies
Keir E. Lewis
Julian M. Hopkin
Kian Fan Chung
Orla O’Carroll
John Faul
Joy Creaser-Thomas
Mark Andrews
Robin Ghosal
Stefan Piatek
Saffron A. G. Willis-Owen
Theda U. P. Bartolomaeus
Till Birkner
Sarah Dwyer
Nitin Kumar
Elena M. Turek
A. William Musk
Jennie Hui
Michael Hunter
Alan James
Marc-Emmanuel Dumas
Sarah Filippi
Michael J. Cox
Trevor D. Lawley
Sofia K. Forslund
Miriam F. Moffatt
William. O. C. Cookson
author_facet Leah Cuthbertson
Ulrike Löber
Jonathan S. Ish-Horowicz
Claire N. McBrien
Colin Churchward
Jeremy C. Parker
Michael T. Olanipekun
Conor Burke
Aisling McGowan
Gwyneth A. Davies
Keir E. Lewis
Julian M. Hopkin
Kian Fan Chung
Orla O’Carroll
John Faul
Joy Creaser-Thomas
Mark Andrews
Robin Ghosal
Stefan Piatek
Saffron A. G. Willis-Owen
Theda U. P. Bartolomaeus
Till Birkner
Sarah Dwyer
Nitin Kumar
Elena M. Turek
A. William Musk
Jennie Hui
Michael Hunter
Alan James
Marc-Emmanuel Dumas
Sarah Filippi
Michael J. Cox
Trevor D. Lawley
Sofia K. Forslund
Miriam F. Moffatt
William. O. C. Cookson
author_sort Leah Cuthbertson
collection DOAJ
description Abstract Microbial communities at the airway mucosal barrier are conserved and highly ordered, in likelihood reflecting co-evolution with human host factors. Freed of selection to digest nutrients, the airway microbiome underpins cognate management of mucosal immunity and pathogen resistance. We show here the initial results of systematic culture and whole-genome sequencing of the thoracic airway bacteria, identifying 52 novel species amongst 126 organisms that constitute 75% of commensals typically present in heathy individuals. Clinically relevant genes encode antimicrobial synthesis, adhesion and biofilm formation, immune modulation, iron utilisation, nitrous oxide (NO) metabolism and sphingolipid signalling. Using whole-genome content we identify dysbiotic features that may influence asthma and chronic obstructive pulmonary disease. We match isolate gene content to transcripts and metabolites expressed late in airway epithelial differentiation, identifying pathways to sustain host interactions with microbiota. Our results provide a systematic basis for decrypting interactions between commensals, pathogens, and mucosa in lung diseases of global significance.
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spelling doaj.art-fa0a86718fb4447f9b20ab7e4ec9f3222024-03-05T19:59:45ZengNature PortfolioCommunications Biology2399-36422024-02-017111410.1038/s42003-024-05840-3Genomic attributes of airway commensal bacteria and mucosaLeah Cuthbertson0Ulrike Löber1Jonathan S. Ish-Horowicz2Claire N. McBrien3Colin Churchward4Jeremy C. Parker5Michael T. Olanipekun6Conor Burke7Aisling McGowan8Gwyneth A. Davies9Keir E. Lewis10Julian M. Hopkin11Kian Fan Chung12Orla O’Carroll13John Faul14Joy Creaser-Thomas15Mark Andrews16Robin Ghosal17Stefan Piatek18Saffron A. G. Willis-Owen19Theda U. P. Bartolomaeus20Till Birkner21Sarah Dwyer22Nitin Kumar23Elena M. Turek24A. William Musk25Jennie Hui26Michael Hunter27Alan James28Marc-Emmanuel Dumas29Sarah Filippi30Michael J. Cox31Trevor D. Lawley32Sofia K. Forslund33Miriam F. Moffatt34William. O. C. Cookson35National Heart and Lung Institute, Imperial College LondonMax Delbrück Center for Molecular Medicine (MDC)National Heart and Lung Institute, Imperial College LondonNational Heart and Lung Institute, Imperial College LondonNational Heart and Lung Institute, Imperial College LondonNational Heart and Lung Institute, Imperial College LondonNational Heart and Lung Institute, Imperial College LondonDepartment of Respiratory Medicine, Connolly HospitalDepartment of Respiratory Medicine, Connolly HospitalPopulation Data Science and Health Data Research UK BREATHE Hub, Swansea University Medical School, Swansea UniversityCollege of Medicine, Institute of Life Science, Swansea UniversityCollege of Medicine, Institute of Life Science, Swansea UniversityNational Heart and Lung Institute, Imperial College LondonDepartment of Respiratory Medicine, Connolly HospitalDepartment of Respiratory Medicine, Connolly HospitalCollege of Medicine, Institute of Life Science, Swansea UniversityRespiratory Medicine, Hywel Dda University Health BoardRespiratory Medicine, Hywel Dda University Health BoardNational Heart and Lung Institute, Imperial College LondonNational Heart and Lung Institute, Imperial College LondonMax Delbrück Center for Molecular Medicine (MDC)Max Delbrück Center for Molecular Medicine (MDC)National Heart and Lung Institute, Imperial College LondonHost-Microbiota Interactions Laboratory, Wellcome Sanger Institute, Wellcome Genome CampusNational Heart and Lung Institute, Imperial College LondonSchool of Population and Global Health, The University of Western AustraliaSchool of Population and Global Health, The University of Western AustraliaSchool of Population and Global Health, The University of Western AustraliaSchool of Population and Global Health, The University of Western AustraliaNational Heart and Lung Institute, Imperial College LondonDepartment of Mathematics, Imperial College LondonUniversity of Birmingham College of Medical and Dental Sciences, 150183, Institute of Microbiology and InfectionHost-Microbiota Interactions Laboratory, Wellcome Sanger Institute, Wellcome Genome CampusMax Delbrück Center for Molecular Medicine (MDC)National Heart and Lung Institute, Imperial College LondonNational Heart and Lung Institute, Imperial College LondonAbstract Microbial communities at the airway mucosal barrier are conserved and highly ordered, in likelihood reflecting co-evolution with human host factors. Freed of selection to digest nutrients, the airway microbiome underpins cognate management of mucosal immunity and pathogen resistance. We show here the initial results of systematic culture and whole-genome sequencing of the thoracic airway bacteria, identifying 52 novel species amongst 126 organisms that constitute 75% of commensals typically present in heathy individuals. Clinically relevant genes encode antimicrobial synthesis, adhesion and biofilm formation, immune modulation, iron utilisation, nitrous oxide (NO) metabolism and sphingolipid signalling. Using whole-genome content we identify dysbiotic features that may influence asthma and chronic obstructive pulmonary disease. We match isolate gene content to transcripts and metabolites expressed late in airway epithelial differentiation, identifying pathways to sustain host interactions with microbiota. Our results provide a systematic basis for decrypting interactions between commensals, pathogens, and mucosa in lung diseases of global significance.https://doi.org/10.1038/s42003-024-05840-3
spellingShingle Leah Cuthbertson
Ulrike Löber
Jonathan S. Ish-Horowicz
Claire N. McBrien
Colin Churchward
Jeremy C. Parker
Michael T. Olanipekun
Conor Burke
Aisling McGowan
Gwyneth A. Davies
Keir E. Lewis
Julian M. Hopkin
Kian Fan Chung
Orla O’Carroll
John Faul
Joy Creaser-Thomas
Mark Andrews
Robin Ghosal
Stefan Piatek
Saffron A. G. Willis-Owen
Theda U. P. Bartolomaeus
Till Birkner
Sarah Dwyer
Nitin Kumar
Elena M. Turek
A. William Musk
Jennie Hui
Michael Hunter
Alan James
Marc-Emmanuel Dumas
Sarah Filippi
Michael J. Cox
Trevor D. Lawley
Sofia K. Forslund
Miriam F. Moffatt
William. O. C. Cookson
Genomic attributes of airway commensal bacteria and mucosa
Communications Biology
title Genomic attributes of airway commensal bacteria and mucosa
title_full Genomic attributes of airway commensal bacteria and mucosa
title_fullStr Genomic attributes of airway commensal bacteria and mucosa
title_full_unstemmed Genomic attributes of airway commensal bacteria and mucosa
title_short Genomic attributes of airway commensal bacteria and mucosa
title_sort genomic attributes of airway commensal bacteria and mucosa
url https://doi.org/10.1038/s42003-024-05840-3
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