Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways

ABSTRACT Genome analyses have documented that there are differences in gene repertoire between evolutionary distant lineages of the same bacterial species; however, less is known about microevolutionary dynamics of gene loss and acquisition within bacterial lineages as they evolve over years. Here,...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Migle Gabrielaite, Helle K. Johansen, Søren Molin, Finn C. Nielsen, Rasmus L. Marvig
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Pseudomonas aeruginosa computational biology evolution genomics host-pathogen interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/84197cb71d2e4dbe9d2b7c9247d203e5
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:84197cb71d2e4dbe9d2b7c9247d203e5
record_format	dspace
spelling	oai:doaj.org-article:84197cb71d2e4dbe9d2b7c9247d203e52021-11-15T16:19:09ZGene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways10.1128/mBio.02359-202150-7511https://doaj.org/article/84197cb71d2e4dbe9d2b7c9247d203e52020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02359-20https://doaj.org/toc/2150-7511ABSTRACT Genome analyses have documented that there are differences in gene repertoire between evolutionary distant lineages of the same bacterial species; however, less is known about microevolutionary dynamics of gene loss and acquisition within bacterial lineages as they evolve over years. Here, we analyzed the genomes of 45 Pseudomonas aeruginosa lineages evolving in the lungs of cystic fibrosis (CF) patients to identify genes that are lost or acquired during the first years of infection. On average, lineage genome content changed by 88 genes (range, 0 to 473). Genes were more often lost than acquired, and prophage genes were more variable than bacterial genes. We identified convergent loss or acquisition of the same genes across lineages, suggesting selection for loss and acquisition of certain genes in the host environment. We found that a notable proportion of such genes are associated with virulence; a trait previously shown to be important for adaptation. Furthermore, we also compared the genomes across lineages to show that the within-lineage variable genes (i.e., genes that had been lost or acquired during the infection) often belonged to genomic content not shared across all lineages. In sum, our analysis adds to the knowledge on the pace and drivers of gene loss and acquisition in bacteria evolving over years in a human host environment and provides a basis to further understand how gene loss and acquisition play roles in lineage differentiation and host adaptation. IMPORTANCE Bacterial airway infections, predominantly caused by P. aeruginosa, are a major cause of mortality and morbidity of CF patients. While short insertions and deletions as well as point mutations occurring during infection are well studied, there is a lack of understanding of how gene loss and acquisition play roles in bacterial adaptation to the human airways. Here, we investigated P. aeruginosa within-host evolution with regard to gene loss and acquisition. We show that during long-term infection P. aeruginosa genomes tend to lose genes, in particular, genes related to virulence. This adaptive strategy allows reduction of the genome size and evasion of the host’s immune response. This knowledge is crucial to understand the basic mutational steps that, on the timescale of years, diversify lineages and adds to the identification of bacterial genetic determinants that have implications for CF disease.Migle GabrielaiteHelle K. JohansenSøren MolinFinn C. NielsenRasmus L. MarvigAmerican Society for MicrobiologyarticlePseudomonas aeruginosacomputational biologyevolutiongenomicshost-pathogen interactionsMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa computational biology evolution genomics host-pathogen interactions Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa computational biology evolution genomics host-pathogen interactions Microbiology QR1-502 Migle Gabrielaite Helle K. Johansen Søren Molin Finn C. Nielsen Rasmus L. Marvig Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways
description	ABSTRACT Genome analyses have documented that there are differences in gene repertoire between evolutionary distant lineages of the same bacterial species; however, less is known about microevolutionary dynamics of gene loss and acquisition within bacterial lineages as they evolve over years. Here, we analyzed the genomes of 45 Pseudomonas aeruginosa lineages evolving in the lungs of cystic fibrosis (CF) patients to identify genes that are lost or acquired during the first years of infection. On average, lineage genome content changed by 88 genes (range, 0 to 473). Genes were more often lost than acquired, and prophage genes were more variable than bacterial genes. We identified convergent loss or acquisition of the same genes across lineages, suggesting selection for loss and acquisition of certain genes in the host environment. We found that a notable proportion of such genes are associated with virulence; a trait previously shown to be important for adaptation. Furthermore, we also compared the genomes across lineages to show that the within-lineage variable genes (i.e., genes that had been lost or acquired during the infection) often belonged to genomic content not shared across all lineages. In sum, our analysis adds to the knowledge on the pace and drivers of gene loss and acquisition in bacteria evolving over years in a human host environment and provides a basis to further understand how gene loss and acquisition play roles in lineage differentiation and host adaptation. IMPORTANCE Bacterial airway infections, predominantly caused by P. aeruginosa, are a major cause of mortality and morbidity of CF patients. While short insertions and deletions as well as point mutations occurring during infection are well studied, there is a lack of understanding of how gene loss and acquisition play roles in bacterial adaptation to the human airways. Here, we investigated P. aeruginosa within-host evolution with regard to gene loss and acquisition. We show that during long-term infection P. aeruginosa genomes tend to lose genes, in particular, genes related to virulence. This adaptive strategy allows reduction of the genome size and evasion of the host’s immune response. This knowledge is crucial to understand the basic mutational steps that, on the timescale of years, diversify lineages and adds to the identification of bacterial genetic determinants that have implications for CF disease.
format	article
author	Migle Gabrielaite Helle K. Johansen Søren Molin Finn C. Nielsen Rasmus L. Marvig
author_facet	Migle Gabrielaite Helle K. Johansen Søren Molin Finn C. Nielsen Rasmus L. Marvig
author_sort	Migle Gabrielaite
title	Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways
title_short	Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways
title_full	Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways
title_fullStr	Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways
title_full_unstemmed	Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways
title_sort	gene loss and acquisition in lineages of <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> evolving in cystic fibrosis patient airways
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/84197cb71d2e4dbe9d2b7c9247d203e5
work_keys_str_mv	AT miglegabrielaite genelossandacquisitioninlineagesofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentevolvingincysticfibrosispatientairways AT hellekjohansen genelossandacquisitioninlineagesofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentevolvingincysticfibrosispatientairways AT sørenmolin genelossandacquisitioninlineagesofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentevolvingincysticfibrosispatientairways AT finncnielsen genelossandacquisitioninlineagesofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentevolvingincysticfibrosispatientairways AT rasmuslmarvig genelossandacquisitioninlineagesofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentevolvingincysticfibrosispatientairways
_version_	1718426911637504000

Gene Loss and Acquisition in Lineages of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Evolving in Cystic Fibrosis Patient Airways

Ejemplares similares