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Lung Microbiota Changes Associated with Chronic Pseudomonas Aeruginosa Lung Infection and the Impact Of Edinburgh Research Explorer Lung Microbiota Changes Associated with Chronic Pseudomonas aeruginosa Lung Infection and the Impact of Intravenous Colistimethate Sodium Citation for published version: Collie, D, Glendinning, L, Govan, J, Wright, S, Thornton, E, Tennant, P, Doherty, C & McLachlan, G 2015, 'Lung Microbiota Changes Associated with Chronic Pseudomonas aeruginosa Lung Infection and the Impact of Intravenous Colistimethate Sodium' PLoS One, vol. 10, no. 11, pp. e0142097. DOI: 10.1371/journal.pone.0142097 Digital Object Identifier (DOI): 10.1371/journal.pone.0142097 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: PLoS One Publisher Rights Statement: © 2015 Collie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 05. Apr. 2019 RESEARCH ARTICLE Lung Microbiota Changes Associated with Chronic Pseudomonas aeruginosa Lung Infection and the Impact of Intravenous Colistimethate Sodium David Collie1*, Laura Glendinning1, John Govan2, Steven Wright1, Elisabeth Thornton1, Peter Tennant1, Catherine Doherty2, Gerry McLachlan1 1 The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, United Kingdom, 2 University of Edinburgh, Medical School, Edinburgh, Scotland, United Kingdom * [email protected] Abstract OPEN ACCESS Background Citation: Collie D, Glendinning L, Govan J, Wright S, Exacerbations associated with chronic lung infection with Pseudomonas aeruginosa are a Thornton E, Tennant P, et al. (2015) Lung Microbiota major contributor to morbidity, mortality and premature death in cystic fibrosis. Such exacer- Changes Associated with Chronic Pseudomonas bations are treated with antibiotics, which generally lead to an improvement in lung function aeruginosa Lung Infection and the Impact of Intravenous Colistimethate Sodium. PLoS ONE 10 and reduced sputum P. aeruginosa density. This potentially suggests a role for the latter in (11): e0142097. doi:10.1371/journal.pone.0142097 the pathogenesis of exacerbations. However, other data suggesting that changes in P. aer- Editor: Mohamed N. Seleem, Purdue University, uginosa sputum culture status may not reliably predict an improvement in clinical status, UNITED STATES and data indicating no significant changes in either total bacterial counts or in P. aeruginosa Received: June 10, 2015 numbers in sputum samples collected prior to pulmonary exacerbation sheds doubt on this assumption. We used our recently developed lung segmental model of chronic Pseudomo- Accepted: October 16, 2015 nas infection in sheep to investigate the lung microbiota changes associated with chronic P. Published: November 6, 2015 aeruginosa lung infection and the impact of systemic therapy with colistimethate sodium Copyright: © 2015 Collie et al. This is an open (CMS). access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any Methodology/Principal Findings medium, provided the original author and source are We collected protected specimen brush (PSB) samples from sheep (n = 8) both prior to and credited. 14 days after establishment of chronic local lung infection with P aeruginosa. Samples were Data Availability Statement: All relevant data are taken from both directly infected lung segments (direct) and segments spatially remote to within the paper and its Supporting Information files. such sites (remote). Four sheep were treated with daily intravenous injections of CMS Funding: This work was funded by the Biological and between days 7 and 14, and four were treated with a placebo. Necropsy examination at d14 Biotechnological Science Research Council (BBSRC; confirmed the presence of chronic local lung infection and lung pathology in every direct www.bbsrc.ac.uk). Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/ lung segment. 56), MRC (MR/K001744/1) and BBSRC (BB/ The predominant orders in lung microbiota communities before infection were Bacillales, J004243/1). The funders had no role in study design, Actinomycetales and Clostridiales. While lung microbiota samples were more likely to share data collection and analysis, decision to publish, or preparation of the manuscript. PLOS ONE | DOI:10.1371/journal.pone.0142097 November 6, 2015 1/21 Chronic Pseudomonas aeruginosa Lung Infection Competing Interests: The authors have declared similarities with other samples derived from the same lung, considerable within- and that no competing interests exist. between-animal heterogeneity could be appreciated. Pseudomonadales joined the aforementioned list of predominant orders in lung micro- biota communities after infection. Whilst treatment with CMS appeared to have little impact on microbial community composition after infection, or the change undergone by communi- ties in reaching that state, when Gram negative organisms (excluding Pseudomonadales) were considered together as a group there was a significant decrease in their relative pro- portion that was only observed in the sheep treated with CMS. With only one exception the reduction was seen in both direct and remote lung segments. This reduction, coupled with generally increasing or stable levels of Pseudomonadales, meant that the proportion of the latter relative to total Gram negative bacteria increased in all bar one direct and one remote lung segment. Conclusions/Significance The proportional increase in Pseudomonadales relative to other Gram negative bacteria in the lungs of sheep treated with systemic CMS highlights the potential for such therapies to inadvertently select or create a niche for bacteria seeding from a persistent source of chronic infection. Introduction Pseudomonas aeruginosa is considered to be the most important pathogen in cystic fibrosis (CF), with up to 60% of adult patients infected (UK CF Registry Annual Data Report 2014 [1]), and is also frequently isolated from patients with bronchiectasis [2]. In CF, early infections with P. aeruginosa can be transient, and can clear spontaneously, but colonization with P. aeru- ginosa usually occurs by the time patients reach their teenage years. In the later stages of infec- tion, there is an adaptive shift from free-swimming planktonic P. aeruginosa to a sessile biofilm mode involving mucoid alginate-producing variants of the original colonising strain [3]. This important and characteristic shift is associated with more frequent and more severe pulmonary exacerbations (PEs) that result in progressive decrements in lung function [4]. P. aeruginosa also dominates chronic infections in a proportion of patients with bronchiec- tasis [5] and in chronic obstructive pulmonary disease (COPD) [6] where there is an increasing association with acute exacerbations. The factors linking chronic P. aeruginosa lung infection to PEs are currently unknown. Cer- tainly studies indicating that there is a reduction of sputum P. aeruginosa density during antibi- otic treatment for PE in CF patients—a change that correlates with an improvement in lung function [7], tend to support a primary role for P aeruginosa. However, other data suggesting that changes in P. aeruginosa sputum culture status may not reliably predict an improvement in clinical status [8], and data indicating no significant changes in either total bacterial counts or in P. aeruginosa numbers in sputum samples collected prior to pulmonary exacerbation [9] sheds doubt on the specific role of P. aeruginosa in PE. Such uncertainty has been added to by recent 16S ribosomal DNA sequencing data. In a recent study of fifteen CF patients followed through 21 pulmonary exacerbations, sputum P. aeruginosa numbers did not increase immedi- ately prior to a PE in CF adults [10]. These findings bear comparison with those of Carmody et al (2013) who found that during PE in CF patients bacterial community diversity and PLOS ONE | DOI:10.1371/journal.pone.0142097 November 6, 2015 2/21 Chronic Pseudomonas aeruginosa Lung Infection bacterial density in sputum samples did not change between baseline and exacerbation [11], and Price et al (2013) who similarly found that total and relative abundance of genera at the population level were remarkably stable for individual patients regardless of clinical status [12]. These studies indicate that there are no generalizable ecological ‘signatures’ of PE in this type of clinical sample. Daniels et al (2013)[13] investigated the relative impact of antibiotics, used predominantly to target P. aeruginosa during acute exacerbations, on other non-pseudomonal species. The rel- ative abundance of viable P. aeruginosa
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