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Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans

BACKGROUND: Burkholderia cenocepacia is a human opportunistic pathogen causing devastating symptoms in patients suffering from immunodeficiency and cystic fibrosis. Out of the 303 B. cenocepacia strains with available genomes, the large majority were isolated from a clinical context. However, severa...

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Autores principales: Wallner, Adrian, King, Eoghan, Ngonkeu, Eddy L. M., Moulin, Lionel, Béna, Gilles
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829993/
https://www.ncbi.nlm.nih.gov/pubmed/31684866
http://dx.doi.org/10.1186/s12864-019-6186-z
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author Wallner, Adrian
King, Eoghan
Ngonkeu, Eddy L. M.
Moulin, Lionel
Béna, Gilles
author_facet Wallner, Adrian
King, Eoghan
Ngonkeu, Eddy L. M.
Moulin, Lionel
Béna, Gilles
author_sort Wallner, Adrian
collection PubMed
description BACKGROUND: Burkholderia cenocepacia is a human opportunistic pathogen causing devastating symptoms in patients suffering from immunodeficiency and cystic fibrosis. Out of the 303 B. cenocepacia strains with available genomes, the large majority were isolated from a clinical context. However, several isolates originate from other environmental sources ranging from aerosols to plant endosphere. Plants can represent reservoirs for human infections as some pathogens can survive and sometimes proliferate in the rhizosphere. We therefore investigated if B. cenocepacia had the same potential. RESULTS: We selected genome sequences from 31 different strains, representative of the diversity of ecological niches of B. cenocepacia, and conducted comparative genomic analyses in the aim of finding specific niche or host-related genetic determinants. Phylogenetic analyses and whole genome average nucleotide identity suggest that strains, registered as B. cenocepacia, belong to at least two different species. Core-genome analyses show that the clade enriched in environmental isolates lacks multiple key virulence factors, which are conserved in the sister clade where most clinical isolates fall, including the highly virulent ET12 lineage. Similarly, several plant associated genes display an opposite distribution between the two clades. Finally, we suggest that B. cenocepacia underwent a host jump from plants/environment to animals, as supported by the phylogenetic analysis. We eventually propose a name for the new species that lacks several genetic traits involved in human virulence. CONCLUSION: Regardless of the method used, our studies resulted in a disunited perspective of the B. cenocepacia species. Strains currently affiliated to this taxon belong to at least two distinct species, one having lost several determining animal virulence factors.
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spelling pubmed-68299932019-11-08 Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans Wallner, Adrian King, Eoghan Ngonkeu, Eddy L. M. Moulin, Lionel Béna, Gilles BMC Genomics Research Article BACKGROUND: Burkholderia cenocepacia is a human opportunistic pathogen causing devastating symptoms in patients suffering from immunodeficiency and cystic fibrosis. Out of the 303 B. cenocepacia strains with available genomes, the large majority were isolated from a clinical context. However, several isolates originate from other environmental sources ranging from aerosols to plant endosphere. Plants can represent reservoirs for human infections as some pathogens can survive and sometimes proliferate in the rhizosphere. We therefore investigated if B. cenocepacia had the same potential. RESULTS: We selected genome sequences from 31 different strains, representative of the diversity of ecological niches of B. cenocepacia, and conducted comparative genomic analyses in the aim of finding specific niche or host-related genetic determinants. Phylogenetic analyses and whole genome average nucleotide identity suggest that strains, registered as B. cenocepacia, belong to at least two different species. Core-genome analyses show that the clade enriched in environmental isolates lacks multiple key virulence factors, which are conserved in the sister clade where most clinical isolates fall, including the highly virulent ET12 lineage. Similarly, several plant associated genes display an opposite distribution between the two clades. Finally, we suggest that B. cenocepacia underwent a host jump from plants/environment to animals, as supported by the phylogenetic analysis. We eventually propose a name for the new species that lacks several genetic traits involved in human virulence. CONCLUSION: Regardless of the method used, our studies resulted in a disunited perspective of the B. cenocepacia species. Strains currently affiliated to this taxon belong to at least two distinct species, one having lost several determining animal virulence factors. BioMed Central 2019-11-04 /pmc/articles/PMC6829993/ /pubmed/31684866 http://dx.doi.org/10.1186/s12864-019-6186-z Text en © The Author(s). 2019 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
Wallner, Adrian
King, Eoghan
Ngonkeu, Eddy L. M.
Moulin, Lionel
Béna, Gilles
Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
title Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
title_full Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
title_fullStr Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
title_full_unstemmed Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
title_short Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
title_sort genomic analyses of burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829993/
https://www.ncbi.nlm.nih.gov/pubmed/31684866
http://dx.doi.org/10.1186/s12864-019-6186-z
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