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Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset

Leah Cuthbertson, Lauren Hatfield, Helen Gavillet, Michelle Hardman, Ryan Marsh, Damian W. Rivett, Christopher van der Gast

Microbiome, Volume: 13, Start page: 140

Swansea University Author: Michelle Hardman

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DOI (Published version): 10.1186/s40168-025-02143-5

Abstract

Background: Acute pulmonary exacerbations (PEx) are associated with increased morbidity and earlier mortality for people living with cystic fibrosis (pwCF). The most common causes of PEx in CF are by bacterial infection and concomitant inflammation leading to progressive airway damage. To draw atten...

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Published in: Microbiome
ISSN: 2049-2618
Published: Springer Nature 2025
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To draw attention to the seriousness of PEx they have been labelled as &#x2018;lung attacks&#x2019;, much like a &#x2018;heart attack&#x2019; for acute myocardial infarction. Treatment typically starts when a pwCF presents with worsening respiratory symptoms. Hence, there is a pressing need to identify indicative biomarkers of PEx onset to allow more timely intervention. Set within an ecological framework, we investigated temporal microbiota dynamics to connect changes in the lung microbiota of pwCF to changes in disease states across a PEx event. Results: Species-time relationships (STR) describe how the richness of a community changes with time, here STRs were used to assess temporal turnover (w) within the lung microbiota of each pwCF (n = 12, mean sample duration 315.9 &#xB1; 42.7 days). STRs were characterised by high interpatient variability, indicating that turnover and hence temporal organization are a personalized feature of the CF lung microbiota. Greater turnover was found to be significantly associated with greater change in lung function with time. When microbiota turnover was examined at a finer scale across each pwCF time series, w-values could clearly be observed to increase in the exacerbation period, then peaking within the treatment period, demonstrating that increases in turnover were not solely a result of perturbations caused by PEx antibiotic interventions. STR w-values have been found to have a remarkable degree of similarity for different organisms, in a variety of habitats and ecosystems, and time lengths (typically not exceeding w = 0.5). Here, we found w-values soon increased beyond that. It was therefore possible to use the departure from that expected norm up to start of treatment to approximate onset of PEx in days (21.2 &#xB1; 8.9 days across the study participants). 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spelling 2025-06-09T14:04:57.8940993 v2 69653 2025-06-09 Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset 48b9a2b8a9c1327be7e0515b16332224 Michelle Hardman Michelle Hardman true false 2025-06-09 Background: Acute pulmonary exacerbations (PEx) are associated with increased morbidity and earlier mortality for people living with cystic fibrosis (pwCF). The most common causes of PEx in CF are by bacterial infection and concomitant inflammation leading to progressive airway damage. To draw attention to the seriousness of PEx they have been labelled as ‘lung attacks’, much like a ‘heart attack’ for acute myocardial infarction. Treatment typically starts when a pwCF presents with worsening respiratory symptoms. Hence, there is a pressing need to identify indicative biomarkers of PEx onset to allow more timely intervention. Set within an ecological framework, we investigated temporal microbiota dynamics to connect changes in the lung microbiota of pwCF to changes in disease states across a PEx event. Results: Species-time relationships (STR) describe how the richness of a community changes with time, here STRs were used to assess temporal turnover (w) within the lung microbiota of each pwCF (n = 12, mean sample duration 315.9 ± 42.7 days). STRs were characterised by high interpatient variability, indicating that turnover and hence temporal organization are a personalized feature of the CF lung microbiota. Greater turnover was found to be significantly associated with greater change in lung function with time. When microbiota turnover was examined at a finer scale across each pwCF time series, w-values could clearly be observed to increase in the exacerbation period, then peaking within the treatment period, demonstrating that increases in turnover were not solely a result of perturbations caused by PEx antibiotic interventions. STR w-values have been found to have a remarkable degree of similarity for different organisms, in a variety of habitats and ecosystems, and time lengths (typically not exceeding w = 0.5). Here, we found w-values soon increased beyond that. It was therefore possible to use the departure from that expected norm up to start of treatment to approximate onset of PEx in days (21.2 ± 8.9 days across the study participants). Conclusions: Here, we illustrate that changes in turnover of the lung microbiota of pwCF can be indicative of PEx onset in considerable advance of when treatment would normally be initiated. This offers translational potential to enable early detection of PEx and consequent timely intervention. Journal Article Microbiome 13 140 Springer Nature 2049-2618 Cystic fibrosis; Lung microbiome; Temporal dynamics; Island biogeography; Species-time relationships; Microbiome ecology; Species turnover; Lung function; Pulmonary exacerbation 7 6 2025 2025-06-07 10.1186/s40168-025-02143-5 COLLEGE NANME COLLEGE CODE Swansea University Another institution paid the OA fee This work was supported by the Cystic Fibrosis Trust (VIA 045) awarded to CvdG and DWR, and by the UK Natural Environment Research Council (NE/H019456/1) awarded to CvdG. 2025-06-09T14:04:57.8940993 2025-06-09T13:50:40.7044511 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Leah Cuthbertson 1 Lauren Hatfield 2 Helen Gavillet 3 Michelle Hardman 4 Ryan Marsh 5 Damian W. Rivett 6 Christopher van der Gast 7 69653__34426__b5f716e859bd4cdca17109467c38a2e1.pdf 40168_2025_Article_2143.pdf 2025-06-09T13:50:40.7042967 Output 2054832 application/pdf Version of Record true © The Author(s) 2025. This article is licensed under a Creative Commons Attribution 4.0 International License (CC BY). true eng http://creativecommons.org/licenses/by/4.0/
title Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
spellingShingle Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
Michelle Hardman
title_short Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
title_full Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
title_fullStr Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
title_full_unstemmed Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
title_sort Species turnover within cystic fibrosis lung microbiota is indicative of acute pulmonary exacerbation onset
author_id_str_mv 48b9a2b8a9c1327be7e0515b16332224
author_id_fullname_str_mv 48b9a2b8a9c1327be7e0515b16332224_***_Michelle Hardman
author Michelle Hardman
author2 Leah Cuthbertson
Lauren Hatfield
Helen Gavillet
Michelle Hardman
Ryan Marsh
Damian W. Rivett
Christopher van der Gast
format Journal article
container_title Microbiome
container_volume 13
container_start_page 140
publishDate 2025
institution Swansea University
issn 2049-2618
doi_str_mv 10.1186/s40168-025-02143-5
publisher Springer Nature
college_str Faculty of Medicine, Health and Life Sciences
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hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
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description Background: Acute pulmonary exacerbations (PEx) are associated with increased morbidity and earlier mortality for people living with cystic fibrosis (pwCF). The most common causes of PEx in CF are by bacterial infection and concomitant inflammation leading to progressive airway damage. To draw attention to the seriousness of PEx they have been labelled as ‘lung attacks’, much like a ‘heart attack’ for acute myocardial infarction. Treatment typically starts when a pwCF presents with worsening respiratory symptoms. Hence, there is a pressing need to identify indicative biomarkers of PEx onset to allow more timely intervention. Set within an ecological framework, we investigated temporal microbiota dynamics to connect changes in the lung microbiota of pwCF to changes in disease states across a PEx event. Results: Species-time relationships (STR) describe how the richness of a community changes with time, here STRs were used to assess temporal turnover (w) within the lung microbiota of each pwCF (n = 12, mean sample duration 315.9 ± 42.7 days). STRs were characterised by high interpatient variability, indicating that turnover and hence temporal organization are a personalized feature of the CF lung microbiota. Greater turnover was found to be significantly associated with greater change in lung function with time. When microbiota turnover was examined at a finer scale across each pwCF time series, w-values could clearly be observed to increase in the exacerbation period, then peaking within the treatment period, demonstrating that increases in turnover were not solely a result of perturbations caused by PEx antibiotic interventions. STR w-values have been found to have a remarkable degree of similarity for different organisms, in a variety of habitats and ecosystems, and time lengths (typically not exceeding w = 0.5). Here, we found w-values soon increased beyond that. It was therefore possible to use the departure from that expected norm up to start of treatment to approximate onset of PEx in days (21.2 ± 8.9 days across the study participants). Conclusions: Here, we illustrate that changes in turnover of the lung microbiota of pwCF can be indicative of PEx onset in considerable advance of when treatment would normally be initiated. This offers translational potential to enable early detection of PEx and consequent timely intervention.
published_date 2025-06-07T05:48:03Z
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