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Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre

BACKGROUND: Chronic lung infections caused by Pseudomonas aeruginosa are a significant cause of morbidity and mortality in people with cystic fibrosis (CF). Shared P. aeruginosa strains, that can be transmitted between patients, are of concern and in Australia the AUST-02 shared strain is predominan...

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Autores principales: Wee, Bryan A., Tai, Anna S., Sherrard, Laura J., Ben Zakour, Nouri L., Hanks, Kirt R., Kidd, Timothy J., Ramsay, Kay A., Lamont, Iain, Whiley, David M., Bell, Scott C., Beatson, Scott A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6117919/
https://www.ncbi.nlm.nih.gov/pubmed/30165811
http://dx.doi.org/10.1186/s12864-018-5018-x
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author Wee, Bryan A.
Tai, Anna S.
Sherrard, Laura J.
Ben Zakour, Nouri L.
Hanks, Kirt R.
Kidd, Timothy J.
Ramsay, Kay A.
Lamont, Iain
Whiley, David M.
Bell, Scott C.
Beatson, Scott A.
author_facet Wee, Bryan A.
Tai, Anna S.
Sherrard, Laura J.
Ben Zakour, Nouri L.
Hanks, Kirt R.
Kidd, Timothy J.
Ramsay, Kay A.
Lamont, Iain
Whiley, David M.
Bell, Scott C.
Beatson, Scott A.
author_sort Wee, Bryan A.
collection PubMed
description BACKGROUND: Chronic lung infections caused by Pseudomonas aeruginosa are a significant cause of morbidity and mortality in people with cystic fibrosis (CF). Shared P. aeruginosa strains, that can be transmitted between patients, are of concern and in Australia the AUST-02 shared strain is predominant in individuals attending CF centres in Queensland and Western Australia. M3L7 is a multidrug resistant sub-type of AUST-02 that was recently identified in a Queensland CF centre and was shown to be associated with poorer clinical outcomes. The main aim of this study was to resolve the relationship of the emergent M3L7 sub-type within the AUST-02 group of strains using whole genome sequencing. RESULTS: A whole genome core phylogeny of 63 isolates indicated that M3L7 is a monophyletic sub-lineage within the context of the broader AUST-02 group. Relatively short branch lengths connected all of the M3L7 isolates. A phylogeny based on nucleotide polymorphisms present across the genome showed that the chronological estimation of the most recent common ancestor was around 2001 (± 3 years). SNP differences between sequential non-hypermutator M3L7 isolates collected 3–4 years apart from five patients suggested both continuous infection of the same strain and cross-infection of some M3L7 variants between patients. The majority of polymorphisms that were characteristic of M3L7 (i.e. acquired after divergence from all other AUST-02 isolates sequenced) were found to produce non-synonymous mutations in virulence and antibiotic resistance genes. CONCLUSIONS: M3L7 has recently diverged from a common ancestor, indicating descent from a single carrier at a CF treatment centre in Australia. Both adaptation to the lung and transmission of M3L7 between adults attending this centre may have contributed to its rapid dissemination. Further genomic investigations are required on multiple intra-sample isolates of this sub-type to decipher potential mechanisms which facilitates its epidemiological success. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5018-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-61179192018-09-05 Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre Wee, Bryan A. Tai, Anna S. Sherrard, Laura J. Ben Zakour, Nouri L. Hanks, Kirt R. Kidd, Timothy J. Ramsay, Kay A. Lamont, Iain Whiley, David M. Bell, Scott C. Beatson, Scott A. BMC Genomics Research Article BACKGROUND: Chronic lung infections caused by Pseudomonas aeruginosa are a significant cause of morbidity and mortality in people with cystic fibrosis (CF). Shared P. aeruginosa strains, that can be transmitted between patients, are of concern and in Australia the AUST-02 shared strain is predominant in individuals attending CF centres in Queensland and Western Australia. M3L7 is a multidrug resistant sub-type of AUST-02 that was recently identified in a Queensland CF centre and was shown to be associated with poorer clinical outcomes. The main aim of this study was to resolve the relationship of the emergent M3L7 sub-type within the AUST-02 group of strains using whole genome sequencing. RESULTS: A whole genome core phylogeny of 63 isolates indicated that M3L7 is a monophyletic sub-lineage within the context of the broader AUST-02 group. Relatively short branch lengths connected all of the M3L7 isolates. A phylogeny based on nucleotide polymorphisms present across the genome showed that the chronological estimation of the most recent common ancestor was around 2001 (± 3 years). SNP differences between sequential non-hypermutator M3L7 isolates collected 3–4 years apart from five patients suggested both continuous infection of the same strain and cross-infection of some M3L7 variants between patients. The majority of polymorphisms that were characteristic of M3L7 (i.e. acquired after divergence from all other AUST-02 isolates sequenced) were found to produce non-synonymous mutations in virulence and antibiotic resistance genes. CONCLUSIONS: M3L7 has recently diverged from a common ancestor, indicating descent from a single carrier at a CF treatment centre in Australia. Both adaptation to the lung and transmission of M3L7 between adults attending this centre may have contributed to its rapid dissemination. Further genomic investigations are required on multiple intra-sample isolates of this sub-type to decipher potential mechanisms which facilitates its epidemiological success. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5018-x) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-30 /pmc/articles/PMC6117919/ /pubmed/30165811 http://dx.doi.org/10.1186/s12864-018-5018-x Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Wee, Bryan A.
Tai, Anna S.
Sherrard, Laura J.
Ben Zakour, Nouri L.
Hanks, Kirt R.
Kidd, Timothy J.
Ramsay, Kay A.
Lamont, Iain
Whiley, David M.
Bell, Scott C.
Beatson, Scott A.
Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
title Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
title_full Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
title_fullStr Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
title_full_unstemmed Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
title_short Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
title_sort whole genome sequencing reveals the emergence of a pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6117919/
https://www.ncbi.nlm.nih.gov/pubmed/30165811
http://dx.doi.org/10.1186/s12864-018-5018-x
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