Genomic attributes of airway commensal bacteria and mucosa

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

doi:10.1038/s42003-024-05840-3

Genomic attributes of airway commensal bacteria and mucosa

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-OwenTheda 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^*

^*Corresponding author for this work

Microbiology and Infection

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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.

Original language	English
Article number	171
Number of pages	14
Journal	Communications Biology
Volume	7
Issue number	1
DOIs	https://doi.org/10.1038/s42003-024-05840-3
Publication status	Published - 12 Feb 2024

Bibliographical note

Acknowledgments:
The culture collection was funded primarily by the Asmarley Trust. Isolate sequencing was funded by the Wellcome Trust (WT098051; WT206194 and 108413/A/15/D), and we thank the Wellcome Sanger Institute Pathogen Informatics and Research Support Facility for supporting this research. Jonathan Ish-Horowicz was the recipient of a Wellcome Trust PhD studentship (215359/Z/19/Z). Bioinformatic investigation of isolated genomic sequences was supported by MDC Berlin DFG SFB1449: “Dynamic Hydrogels”; KFO339; “FOOD@“; DFG SFB1365: “Renoprotection”; and JPI-AMR: EMBARK. Genomic studies of airway transcripts were supported by a joint Wellcome Senior Investigator Award to WOCC and MFM (WT096964MA and WT097117MA). The Busselton Healthy Ageing Study is funded by grants from the Government of Western Australia (Office of Science, Department of Health) and the City of Busselton, and from private donations to the Busselton Population Medical Research Institute. We thank the WA Country Health Service and the community of Busselton for their ongoing support and participation.

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Cuthbertson, L., Löber, U., Ish-Horowicz, J. S., McBrien, C. N., Churchward, C., Parker, J. C., Olanipekun, M. T., Burke, C., McGowan, A., Davies, G. A., Lewis, K. E., Hopkin, J. M., Chung, K. F., O’Carroll, O., Faul, J., Creaser-Thomas, J., Andrews, M., Ghosal, R., Piatek, S., ... Cookson, W. O. C. (2024). Genomic attributes of airway commensal bacteria and mucosa. Communications Biology, 7(1), Article 171. https://doi.org/10.1038/s42003-024-05840-3

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title = "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 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.",

author = "Leah Cuthbertson and Ulrike L{\"o}ber and Ish-Horowicz, {Jonathan S.} and McBrien, {Claire N.} and Colin Churchward and Parker, {Jeremy C.} and Olanipekun, {Michael T.} and Conor Burke and Aisling McGowan and Davies, {Gwyneth A.} and Lewis, {Keir E.} and Hopkin, {Julian M.} and Chung, {Kian Fan} and Orla O{\textquoteright}Carroll and John Faul and Joy Creaser-Thomas and Mark Andrews and Robin Ghosal and Stefan Piatek and Willis-Owen, {Saffron A. G.} and Bartolomaeus, {Theda U. P.} and Till Birkner and Sarah Dwyer and Nitin Kumar and Turek, {Elena M.} and {William Musk}, A. and Jennie Hui and Michael Hunter and Alan James and Marc-Emmanuel Dumas and Sarah Filippi and Cox, {Michael J.} and Lawley, {Trevor D.} and Forslund, {Sofia K.} and Moffatt, {Miriam F.} and Cookson, {William. O. C.}",

note = "Acknowledgments: The culture collection was funded primarily by the Asmarley Trust. Isolate sequencing was funded by the Wellcome Trust (WT098051; WT206194 and 108413/A/15/D), and we thank the Wellcome Sanger Institute Pathogen Informatics and Research Support Facility for supporting this research. Jonathan Ish-Horowicz was the recipient of a Wellcome Trust PhD studentship (215359/Z/19/Z). Bioinformatic investigation of isolated genomic sequences was supported by MDC Berlin DFG SFB1449: “Dynamic Hydrogels”; KFO339; “FOOD@“; DFG SFB1365: “Renoprotection”; and JPI-AMR: EMBARK. Genomic studies of airway transcripts were supported by a joint Wellcome Senior Investigator Award to WOCC and MFM (WT096964MA and WT097117MA). The Busselton Healthy Ageing Study is funded by grants from the Government of Western Australia (Office of Science, Department of Health) and the City of Busselton, and from private donations to the Busselton Population Medical Research Institute. We thank the WA Country Health Service and the community of Busselton for their ongoing support and participation.",

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doi = "10.1038/s42003-024-05840-3",

language = "English",

volume = "7",

journal = "Communications Biology",

issn = "2399-3642",

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Cuthbertson, L, Löber, U, Ish-Horowicz, JS, McBrien, CN, Churchward, C, Parker, JC, Olanipekun, MT, Burke, C, McGowan, A, Davies, GA, Lewis, KE, Hopkin, JM, Chung, KF, O’Carroll, O, Faul, J, Creaser-Thomas, J, Andrews, M, Ghosal, R, Piatek, S, Willis-Owen, SAG, Bartolomaeus, TUP, Birkner, T, Dwyer, S, Kumar, N, Turek, EM, William Musk, A, Hui, J, Hunter, M, James, A, Dumas, M-E, Filippi, S, Cox, MJ, Lawley, TD, Forslund, SK, Moffatt, MF & Cookson, WOC 2024, 'Genomic attributes of airway commensal bacteria and mucosa', Communications Biology, vol. 7, no. 1, 171. https://doi.org/10.1038/s42003-024-05840-3

TY - JOUR

T1 - Genomic attributes of airway commensal bacteria and mucosa

AU - Cuthbertson, Leah

AU - Löber, Ulrike

AU - Ish-Horowicz, Jonathan S.

AU - McBrien, Claire N.

AU - Churchward, Colin

AU - Parker, Jeremy C.

AU - Olanipekun, Michael T.

AU - Burke, Conor

AU - McGowan, Aisling

AU - Davies, Gwyneth A.

AU - Lewis, Keir E.

AU - Hopkin, Julian M.

AU - Chung, Kian Fan

AU - O’Carroll, Orla

AU - Faul, John

AU - Creaser-Thomas, Joy

AU - Andrews, Mark

AU - Ghosal, Robin

AU - Piatek, Stefan

AU - Willis-Owen, Saffron A. G.

AU - Bartolomaeus, Theda U. P.

AU - Birkner, Till

AU - Dwyer, Sarah

AU - Kumar, Nitin

AU - Turek, Elena M.

AU - William Musk, A.

AU - Hui, Jennie

AU - Hunter, Michael

AU - James, Alan

AU - Dumas, Marc-Emmanuel

AU - Filippi, Sarah

AU - Cox, Michael J.

AU - Lawley, Trevor D.

AU - Forslund, Sofia K.

AU - Moffatt, Miriam F.

AU - Cookson, William. O. C.

N1 - Acknowledgments: The culture collection was funded primarily by the Asmarley Trust. Isolate sequencing was funded by the Wellcome Trust (WT098051; WT206194 and 108413/A/15/D), and we thank the Wellcome Sanger Institute Pathogen Informatics and Research Support Facility for supporting this research. Jonathan Ish-Horowicz was the recipient of a Wellcome Trust PhD studentship (215359/Z/19/Z). Bioinformatic investigation of isolated genomic sequences was supported by MDC Berlin DFG SFB1449: “Dynamic Hydrogels”; KFO339; “FOOD@“; DFG SFB1365: “Renoprotection”; and JPI-AMR: EMBARK. Genomic studies of airway transcripts were supported by a joint Wellcome Senior Investigator Award to WOCC and MFM (WT096964MA and WT097117MA). The Busselton Healthy Ageing Study is funded by grants from the Government of Western Australia (Office of Science, Department of Health) and the City of Busselton, and from private donations to the Busselton Population Medical Research Institute. We thank the WA Country Health Service and the community of Busselton for their ongoing support and participation.

PY - 2024/2/12

Y1 - 2024/2/12

N2 - 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.

AB - 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.

U2 - 10.1038/s42003-024-05840-3

DO - 10.1038/s42003-024-05840-3

M3 - Article

SN - 2399-3642

VL - 7

JO - Communications Biology

JF - Communications Biology

IS - 1

M1 - 171

ER -

Genomic attributes of airway commensal bacteria and mucosa

Abstract

Bibliographical note

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