Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients.

Lars Jelsbak; Helle Krogh Johansen; Anne-Louise Frost; Regitze Thøgersen; Line E Thomsen; Oana Ciofu; Lei Yang; Janus A J Haagensen; Niels Høiby; Søren Molin

doi:10.1128/IAI.01282-06

Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients.

Lars Jelsbak, Helle Krogh Johansen, Anne-Louise Frost, Regitze Thøgersen, Line E Thomsen, Oana Ciofu, Lei Yang, Janus A J Haagensen, Niels Høiby, Søren Molin

Department of Immunology and Microbiology

170 Citations (Scopus)

Abstract

The ability to establish lifelong persistent infections is a fundamental aspect of the interactions between many pathogenic microorganisms and their mammalian hosts. One example is chronic lung infections by the opportunistic pathogen Pseudomonas aeruginosa in cystic fibrosis (CF) patients. This infection process is associated with extensive genetic adaptation and microevolution of the infecting bacteria. Through investigations of P. aeruginosa populations and infection dynamics in a group of CF patients followed at the Danish CF Clinic in Copenhagen, we have identified two distinct and dominant clones that have evolved into highly successful colonizers of CF patient airways. A significant component of the evolutionary success of these two clones has been their efficient transmissibility among the CF patients. The two clones have been present and transmitted among different CF patients for more than 2 decades. Our data also suggest that the P. aeruginosa population structure in the CF patient airways has been influenced by competition between different clones and that the two dominant clones have been particularly competitive within the lungs, which may add to their overall establishment success. In contrast, we show that adaptive traits commonly associated with establishment of chronic P. aeruginosa infections of CF patients, such as transition to the mucoid phenotype and production of virulence factors, play minor roles in the ability of the two dominant clones to spread among patients and cause long-term chronic infections. These findings suggest that hitherto-unrecognized evolutionary pathways may be involved in the development of successful and persistent P. aeruginosa colonizers of CF patient lungs.

Original language	English
Journal	Infection and Immunity
Volume	75
Issue number	5
Pages (from-to)	2214-24
Number of pages	10
ISSN	0019-9567
DOIs	https://doi.org/10.1128/IAI.01282-06
Publication status	Published - 2007

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title = "Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients.",

abstract = "The ability to establish lifelong persistent infections is a fundamental aspect of the interactions between many pathogenic microorganisms and their mammalian hosts. One example is chronic lung infections by the opportunistic pathogen Pseudomonas aeruginosa in cystic fibrosis (CF) patients. This infection process is associated with extensive genetic adaptation and microevolution of the infecting bacteria. Through investigations of P. aeruginosa populations and infection dynamics in a group of CF patients followed at the Danish CF Clinic in Copenhagen, we have identified two distinct and dominant clones that have evolved into highly successful colonizers of CF patient airways. A significant component of the evolutionary success of these two clones has been their efficient transmissibility among the CF patients. The two clones have been present and transmitted among different CF patients for more than 2 decades. Our data also suggest that the P. aeruginosa population structure in the CF patient airways has been influenced by competition between different clones and that the two dominant clones have been particularly competitive within the lungs, which may add to their overall establishment success. In contrast, we show that adaptive traits commonly associated with establishment of chronic P. aeruginosa infections of CF patients, such as transition to the mucoid phenotype and production of virulence factors, play minor roles in the ability of the two dominant clones to spread among patients and cause long-term chronic infections. These findings suggest that hitherto-unrecognized evolutionary pathways may be involved in the development of successful and persistent P. aeruginosa colonizers of CF patient lungs.",

author = "Lars Jelsbak and Johansen, {Helle Krogh} and Anne-Louise Frost and Regitze Th{\o}gersen and Thomsen, {Line E} and Oana Ciofu and Lei Yang and Haagensen, {Janus A J} and Niels H{\o}iby and S{\o}ren Molin",

note = "Keywords: Adolescent; Adult; Child; Child, Preschool; Chronic Disease; Cystic Fibrosis; Denmark; Electrophoresis, Gel, Pulsed-Field; Epidemiology, Molecular; Female; Genotype; Humans; Lung; Male; Pseudomonas Infections; Pseudomonas aeruginosa; Variation (Genetics)",

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AU - Jelsbak, Lars

AU - Johansen, Helle Krogh

AU - Frost, Anne-Louise

AU - Thøgersen, Regitze

AU - Thomsen, Line E

AU - Ciofu, Oana

AU - Yang, Lei

AU - Haagensen, Janus A J

AU - Høiby, Niels

AU - Molin, Søren

N1 - Keywords: Adolescent; Adult; Child; Child, Preschool; Chronic Disease; Cystic Fibrosis; Denmark; Electrophoresis, Gel, Pulsed-Field; Epidemiology, Molecular; Female; Genotype; Humans; Lung; Male; Pseudomonas Infections; Pseudomonas aeruginosa; Variation (Genetics)

PY - 2007

Y1 - 2007

N2 - The ability to establish lifelong persistent infections is a fundamental aspect of the interactions between many pathogenic microorganisms and their mammalian hosts. One example is chronic lung infections by the opportunistic pathogen Pseudomonas aeruginosa in cystic fibrosis (CF) patients. This infection process is associated with extensive genetic adaptation and microevolution of the infecting bacteria. Through investigations of P. aeruginosa populations and infection dynamics in a group of CF patients followed at the Danish CF Clinic in Copenhagen, we have identified two distinct and dominant clones that have evolved into highly successful colonizers of CF patient airways. A significant component of the evolutionary success of these two clones has been their efficient transmissibility among the CF patients. The two clones have been present and transmitted among different CF patients for more than 2 decades. Our data also suggest that the P. aeruginosa population structure in the CF patient airways has been influenced by competition between different clones and that the two dominant clones have been particularly competitive within the lungs, which may add to their overall establishment success. In contrast, we show that adaptive traits commonly associated with establishment of chronic P. aeruginosa infections of CF patients, such as transition to the mucoid phenotype and production of virulence factors, play minor roles in the ability of the two dominant clones to spread among patients and cause long-term chronic infections. These findings suggest that hitherto-unrecognized evolutionary pathways may be involved in the development of successful and persistent P. aeruginosa colonizers of CF patient lungs.

AB - The ability to establish lifelong persistent infections is a fundamental aspect of the interactions between many pathogenic microorganisms and their mammalian hosts. One example is chronic lung infections by the opportunistic pathogen Pseudomonas aeruginosa in cystic fibrosis (CF) patients. This infection process is associated with extensive genetic adaptation and microevolution of the infecting bacteria. Through investigations of P. aeruginosa populations and infection dynamics in a group of CF patients followed at the Danish CF Clinic in Copenhagen, we have identified two distinct and dominant clones that have evolved into highly successful colonizers of CF patient airways. A significant component of the evolutionary success of these two clones has been their efficient transmissibility among the CF patients. The two clones have been present and transmitted among different CF patients for more than 2 decades. Our data also suggest that the P. aeruginosa population structure in the CF patient airways has been influenced by competition between different clones and that the two dominant clones have been particularly competitive within the lungs, which may add to their overall establishment success. In contrast, we show that adaptive traits commonly associated with establishment of chronic P. aeruginosa infections of CF patients, such as transition to the mucoid phenotype and production of virulence factors, play minor roles in the ability of the two dominant clones to spread among patients and cause long-term chronic infections. These findings suggest that hitherto-unrecognized evolutionary pathways may be involved in the development of successful and persistent P. aeruginosa colonizers of CF patient lungs.

U2 - 10.1128/IAI.01282-06

DO - 10.1128/IAI.01282-06

M3 - Journal article

C2 - 17261614

SN - 0019-9567

VL - 75

SP - 2214

EP - 2224

JO - Infection and Immunity

JF - Infection and Immunity

IS - 5

ER -

Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients.

Abstract

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