Lung function and microbiota diversity in cystic fibrosis

Leah Cuthbertson, Alan W. Walker, Anna E. Oliver, Geraint B. Rogers, Damian W. Rivett, Thomas H. Hampton, Alix Ashare, J. Stuart Elborn, Anthony De Soyza, Mary P. Carroll, Lucas R. Hoffman, Clare Lanyon, Samuel M. Moskowitz, George A. O'Toole, Julian Parkhill, Paul J. Planet, Charlotte C. Teneback, Michael M. Tunney, Jonathan B. Zuckerman, Kenneth D. BruceChristopher J. Van Der Gast

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Abstract

Background: Chronic infection and concomitant airway inflammation is the leading cause of morbidity and mortality for people living with cystic fibrosis (CF). Although chronic infection in CF is undeniably polymicrobial, involving a lung microbiota, infection surveillance and control approaches remain underpinned by classical aerobic culture-based microbiology. How to use microbiomics to direct clinical management of CF airway infections remains a crucial challenge. A pivotal step towards leveraging microbiome approaches in CF clinical care is to understand the ecology of the CF lung microbiome and identify ecological patterns of CF microbiota across a wide spectrum of lung disease. Assessing sputum samples from 299 patients attending 13 CF centres in Europe and the USA, we determined whether the emerging relationship of decreasing microbiota diversity with worsening lung function could be considered a generalised pattern of CF lung microbiota and explored its potential as an informative indicator of lung disease state in CF. Results: We tested and found decreasing microbiota diversity with a reduction in lung function to be a significant ecological pattern. Moreover, the loss of diversity was accompanied by an increase in microbiota dominance. Subsequently, we stratified patients into lung disease categories of increasing disease severity to further investigate relationships between microbiota characteristics and lung function, and the factors contributing to microbiota variance. Core taxa group composition became highly conserved within the severe disease category, while the rarer satellite taxa underpinned the high variability observed in the microbiota diversity. Further, the lung microbiota of individual patient were increasingly dominated by recognised CF pathogens as lung function decreased. Conversely, other bacteria, especially obligate anaerobes, increasingly dominated in those with better lung function. Ordination analyses revealed lung function and antibiotics to be main explanators of compositional variance in the microbiota and the core and satellite taxa. Biogeography was found to influence acquisition of the rarer satellite taxa. Conclusions: Our findings demonstrate that microbiota diversity and dominance, as well as the identity of the dominant bacterial species, in combination with measures of lung function, can be used as informative indicators of disease state in CF. [MediaObject not available: see fulltext.]

Original languageEnglish
Article number45
Number of pages13
JournalMicrobiome
Volume8
DOIs
Publication statusPublished - 2 Apr 2020

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© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons
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Keywords

  • Antibiotics
  • Biogeography
  • Cystic fibrosis
  • Disease severity
  • Ecological patterns
  • Lung function
  • Lung microbiome
  • Lung microbiota
  • Microbial surveillance

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    Cuthbertson, L., Walker, A. W., Oliver, A. E., Rogers, G. B., Rivett, D. W., Hampton, T. H., Ashare, A., Elborn, J. S., De Soyza, A., Carroll, M. P., Hoffman, L. R., Lanyon, C., Moskowitz, S. M., O'Toole, G. A., Parkhill, J., Planet, P. J., Teneback, C. C., Tunney, M. M., Zuckerman, J. B., ... Van Der Gast, C. J. (2020). Lung function and microbiota diversity in cystic fibrosis. Microbiome, 8, [45]. https://doi.org/10.1186/s40168-020-00810-3