Early life inter-kingdom interactions shape the immunological environment of the airways
Early life inter-kingdom interactions shape the immunological environment of the airways
Background: there is increasing evidence that the airway microbiome plays a key role in the establishment of respiratory health by interacting with the developing immune system early in life. While it has become clear that bacteria are involved in this process, there is a knowledge gap concerning the role of fungi. Moreover, the inter-kingdom interactions that influence immune development remain unknown. In this prospective exploratory human study, we aimed to determine early post-natal microbial and immunological features of the upper airways in 121 healthy newborns.
Results: we found that the oropharynx and nasal cavity represent distinct ecological niches for bacteria and fungi. Breastfeeding correlated with changes in microbiota composition of oropharyngeal samples with the greatest impact upon the relative abundance of Streptococcus species and Candida. Host transcriptome profiling revealed that genes with the highest expression variation were immunological in nature. Multi-omics factor analysis of host and microbial data revealed unique co-variation patterns.
Conclusion: these data provide evidence of a diverse multi-kingdom microbiota linked with local immunological characteristics in the first week of life that could represent distinct trajectories for future respiratory health.
Trial registration: NHS Health Research Authority, IRAS ID 199053. Registered 5 Oct 2016. https://www.hra.nhs.uk/planning-and-improving-research/application-summaries/research-summaries/breathing-together/ [MediaObject not available: see fulltext.]
Pattaroni, Céline
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Macowan, Matthew
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Chatzis, Roxanne
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Daunt, Carmel
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Custovic, Adnan
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Shields, Michael D
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Power, Ultan F
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Grigg, Jonathan
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Roberts, Graham
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Ghazal, Peter
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Schwarze, Jürgen
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Gore, Mindy
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Turner, Steve
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Bush, Andrew
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Saglani, Sejal
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Lloyd, Clare M
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Marsland, Benjamin J
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21 February 2022
Pattaroni, Céline
25092aed-88a8-4c20-9913-11a0e223373e
Macowan, Matthew
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Chatzis, Roxanne
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Daunt, Carmel
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Custovic, Adnan
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Shields, Michael D
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Power, Ultan F
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Grigg, Jonathan
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Roberts, Graham
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Ghazal, Peter
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Schwarze, Jürgen
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Gore, Mindy
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Turner, Steve
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Bush, Andrew
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Saglani, Sejal
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Lloyd, Clare M
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Marsland, Benjamin J
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Pattaroni, Céline, Macowan, Matthew, Chatzis, Roxanne, Daunt, Carmel, Custovic, Adnan, Shields, Michael D, Power, Ultan F, Grigg, Jonathan, Roberts, Graham, Ghazal, Peter, Schwarze, Jürgen, Gore, Mindy, Turner, Steve, Bush, Andrew, Saglani, Sejal, Lloyd, Clare M and Marsland, Benjamin J
(2022)
Early life inter-kingdom interactions shape the immunological environment of the airways.
Microbiome, 10 (1), [34].
(doi:10.1186/s40168-021-01201-y).
Abstract
Background: there is increasing evidence that the airway microbiome plays a key role in the establishment of respiratory health by interacting with the developing immune system early in life. While it has become clear that bacteria are involved in this process, there is a knowledge gap concerning the role of fungi. Moreover, the inter-kingdom interactions that influence immune development remain unknown. In this prospective exploratory human study, we aimed to determine early post-natal microbial and immunological features of the upper airways in 121 healthy newborns.
Results: we found that the oropharynx and nasal cavity represent distinct ecological niches for bacteria and fungi. Breastfeeding correlated with changes in microbiota composition of oropharyngeal samples with the greatest impact upon the relative abundance of Streptococcus species and Candida. Host transcriptome profiling revealed that genes with the highest expression variation were immunological in nature. Multi-omics factor analysis of host and microbial data revealed unique co-variation patterns.
Conclusion: these data provide evidence of a diverse multi-kingdom microbiota linked with local immunological characteristics in the first week of life that could represent distinct trajectories for future respiratory health.
Trial registration: NHS Health Research Authority, IRAS ID 199053. Registered 5 Oct 2016. https://www.hra.nhs.uk/planning-and-improving-research/application-summaries/research-summaries/breathing-together/ [MediaObject not available: see fulltext.]
Text
s40168-021-01201-y
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More information
Accepted/In Press date: 12 November 2021
Published date: 21 February 2022
Additional Information:
Funding Information:
We are grateful to the infants of the cohort and their families for participating in this study as well as all the Breathing Together team. We would like to thank Scott Maxwell of the Department of Diabetes and Helen Mitchell from the Alfred Research Alliance Sequencing Platform for their help with sequencing and technical support as well as Nick Wong from the Monash Bioinformatics platform for RNAseq analysis insights. This work was supported by the MASSIVE HPC facility (www.massive.org.au).
Funding Information:
We are grateful to the infants of the cohort and their families for participating in this study as well as all the Breathing Together team. We would like to thank Scott Maxwell of the Department of Diabetes and Helen Mitchell from the Alfred Research Alliance Sequencing Platform for their help with sequencing and technical support as well as Nick Wong from the Monash Bioinformatics platform for RNAseq analysis insights. This work was supported by the MASSIVE HPC facility ( www.massive.org.au ).
Publisher Copyright:
© 2022, The Author(s).
Copyright:
Copyright 2022 Elsevier B.V., All rights reserved.
Identifiers
Local EPrints ID: 455421
URI: http://eprints.soton.ac.uk/id/eprint/455421
ISSN: 2049-2618
PURE UUID: 4a6f7ce9-62a5-4c76-8c1f-7e5a6178b455
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Date deposited: 21 Mar 2022 17:49
Last modified: 17 Mar 2024 03:02
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Contributors
Author:
Céline Pattaroni
Author:
Matthew Macowan
Author:
Roxanne Chatzis
Author:
Carmel Daunt
Author:
Adnan Custovic
Author:
Michael D Shields
Author:
Ultan F Power
Author:
Jonathan Grigg
Author:
Peter Ghazal
Author:
Jürgen Schwarze
Author:
Mindy Gore
Author:
Steve Turner
Author:
Andrew Bush
Author:
Sejal Saglani
Author:
Clare M Lloyd
Author:
Benjamin J Marsland
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