The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients

Matthew T G Holden; Helena M B Seth-Smith; Lisa C Crossman; Mohammed Sebaihia; Stephen D Bentley; Ana M Cerdeño-Tárraga; Nicholas R Thomson; Nathalie Bason; Michael A Quail; Sarah Sharp; Inna Cherevach; Carol Churcher; Ian Goodhead; Heidi Hauser; Nancy Holroyd; Karen Mungall; Paul Scott; Danielle Walker; Brian White; Helen Rose; Pernille Iversen; Dalila Mil-Homens; Eduardo P C Rocha; Arsenio M Fialho; Adam Baldwin; Christopher Dowson; Bart G Barrell; John R Govan; Peter Vandamme; C Anthony Hart; Eshwar Mahenthiralingam; Julian Parkhill

doi:10.1128/JB.01230-08

The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients

Matthew T G Holden, Helena M B Seth-Smith, Lisa C Crossman, Mohammed Sebaihia, Stephen D Bentley, Ana M Cerdeño-Tárraga, Nicholas R Thomson, Nathalie Bason, Michael A Quail, Sarah Sharp, Inna Cherevach, Carol Churcher, Ian Goodhead, Heidi Hauser, Nancy Holroyd, Karen Mungall, Paul Scott, Danielle Walker, Brian White, Helen RosePernille Iversen, Dalila Mil-Homens, Eduardo P C Rocha, Arsenio M Fialho, Adam Baldwin, Christopher Dowson, Bart G Barrell, John R Govan, Peter Vandamme, C Anthony Hart, Eshwar Mahenthiralingam, Julian Parkhill

Functional Genomics

242 Citations (Scopus)

Abstract

Bacterial infections of the lungs of cystic fibrosis (CF) patients cause major complications in the treatment of this common genetic disease. Burkholderia cenocepacia infection is particularly problematic since this organism has high levels of antibiotic resistance, making it difficult to eradicate; the resulting chronic infections are associated with severe declines in lung function and increased mortality rates. B. cenocepacia strain J2315 was isolated from a CF patient and is a member of the epidemic ET12 lineage that originated in Canada or the United Kingdom and spread to Europe. The 8.06-Mb genome of this highly transmissible pathogen comprises three circular chromosomes and a plasmid and encodes a broad array of functions typical of this metabolically versatile genus, as well as numerous virulence and drug resistance functions. Although B. cenocepacia strains can be isolated from soil and can be pathogenic to both plants and man, J2315 is representative of a lineage of B. cenocepacia rarely isolated from the environment and which spreads between CF patients. Comparative analysis revealed that ca. 21% of the genome is unique in comparison to other strains of B. cenocepacia, highlighting the genomic plasticity of this species. Pseudogenes in virulence determinants suggest that the pathogenic response of J2315 may have been recently selected to promote persistence in the CF lung. The J2315 genome contains evidence that its unique and highly adapted genetic content has played a significant role in its success as an epidemic CF pathogen.

Original language	English
Journal	Journal of Bacteriology
Volume	191
Issue number	1
Pages (from-to)	261-77
Number of pages	16
ISSN	0021-9193
DOIs	https://doi.org/10.1128/JB.01230-08
Publication status	Published - 2009

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Holden, M. T. G., Seth-Smith, H. M. B., Crossman, L. C., Sebaihia, M., Bentley, S. D., Cerdeño-Tárraga, A. M., Thomson, N. R., Bason, N., Quail, M. A., Sharp, S., Cherevach, I., Churcher, C., Goodhead, I., Hauser, H., Holroyd, N., Mungall, K., Scott, P., Walker, D., White, B., ... Parkhill, J. (2009). The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. Journal of Bacteriology, 191(1), 261-77. https://doi.org/10.1128/JB.01230-08

Holden, MTG, Seth-Smith, HMB, Crossman, LC, Sebaihia, M, Bentley, SD, Cerdeño-Tárraga, AM, Thomson, NR, Bason, N, Quail, MA, Sharp, S, Cherevach, I, Churcher, C, Goodhead, I, Hauser, H, Holroyd, N, Mungall, K, Scott, P, Walker, D, White, B, Rose, H, Iversen, P, Mil-Homens, D, Rocha, EPC, Fialho, AM, Baldwin, A, Dowson, C, Barrell, BG, Govan, JR, Vandamme, P, Hart, CA, Mahenthiralingam, E & Parkhill, J 2009, 'The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients', Journal of Bacteriology, vol. 191, no. 1, pp. 261-77. https://doi.org/10.1128/JB.01230-08

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title = "The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients",

abstract = "Bacterial infections of the lungs of cystic fibrosis (CF) patients cause major complications in the treatment of this common genetic disease. Burkholderia cenocepacia infection is particularly problematic since this organism has high levels of antibiotic resistance, making it difficult to eradicate; the resulting chronic infections are associated with severe declines in lung function and increased mortality rates. B. cenocepacia strain J2315 was isolated from a CF patient and is a member of the epidemic ET12 lineage that originated in Canada or the United Kingdom and spread to Europe. The 8.06-Mb genome of this highly transmissible pathogen comprises three circular chromosomes and a plasmid and encodes a broad array of functions typical of this metabolically versatile genus, as well as numerous virulence and drug resistance functions. Although B. cenocepacia strains can be isolated from soil and can be pathogenic to both plants and man, J2315 is representative of a lineage of B. cenocepacia rarely isolated from the environment and which spreads between CF patients. Comparative analysis revealed that ca. 21% of the genome is unique in comparison to other strains of B. cenocepacia, highlighting the genomic plasticity of this species. Pseudogenes in virulence determinants suggest that the pathogenic response of J2315 may have been recently selected to promote persistence in the CF lung. The J2315 genome contains evidence that its unique and highly adapted genetic content has played a significant role in its success as an epidemic CF pathogen.",

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AU - Holden, Matthew T G

AU - Seth-Smith, Helena M B

AU - Crossman, Lisa C

AU - Sebaihia, Mohammed

AU - Bentley, Stephen D

AU - Cerdeño-Tárraga, Ana M

AU - Thomson, Nicholas R

AU - Bason, Nathalie

AU - Quail, Michael A

AU - Sharp, Sarah

AU - Cherevach, Inna

AU - Churcher, Carol

AU - Goodhead, Ian

AU - Hauser, Heidi

AU - Holroyd, Nancy

AU - Mungall, Karen

AU - Scott, Paul

AU - Walker, Danielle

AU - White, Brian

AU - Rose, Helen

AU - Iversen, Pernille

AU - Mil-Homens, Dalila

AU - Rocha, Eduardo P C

AU - Fialho, Arsenio M

AU - Baldwin, Adam

AU - Dowson, Christopher

AU - Barrell, Bart G

AU - Govan, John R

AU - Vandamme, Peter

AU - Hart, C Anthony

AU - Mahenthiralingam, Eshwar

AU - Parkhill, Julian

PY - 2009

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N2 - Bacterial infections of the lungs of cystic fibrosis (CF) patients cause major complications in the treatment of this common genetic disease. Burkholderia cenocepacia infection is particularly problematic since this organism has high levels of antibiotic resistance, making it difficult to eradicate; the resulting chronic infections are associated with severe declines in lung function and increased mortality rates. B. cenocepacia strain J2315 was isolated from a CF patient and is a member of the epidemic ET12 lineage that originated in Canada or the United Kingdom and spread to Europe. The 8.06-Mb genome of this highly transmissible pathogen comprises three circular chromosomes and a plasmid and encodes a broad array of functions typical of this metabolically versatile genus, as well as numerous virulence and drug resistance functions. Although B. cenocepacia strains can be isolated from soil and can be pathogenic to both plants and man, J2315 is representative of a lineage of B. cenocepacia rarely isolated from the environment and which spreads between CF patients. Comparative analysis revealed that ca. 21% of the genome is unique in comparison to other strains of B. cenocepacia, highlighting the genomic plasticity of this species. Pseudogenes in virulence determinants suggest that the pathogenic response of J2315 may have been recently selected to promote persistence in the CF lung. The J2315 genome contains evidence that its unique and highly adapted genetic content has played a significant role in its success as an epidemic CF pathogen.

AB - Bacterial infections of the lungs of cystic fibrosis (CF) patients cause major complications in the treatment of this common genetic disease. Burkholderia cenocepacia infection is particularly problematic since this organism has high levels of antibiotic resistance, making it difficult to eradicate; the resulting chronic infections are associated with severe declines in lung function and increased mortality rates. B. cenocepacia strain J2315 was isolated from a CF patient and is a member of the epidemic ET12 lineage that originated in Canada or the United Kingdom and spread to Europe. The 8.06-Mb genome of this highly transmissible pathogen comprises three circular chromosomes and a plasmid and encodes a broad array of functions typical of this metabolically versatile genus, as well as numerous virulence and drug resistance functions. Although B. cenocepacia strains can be isolated from soil and can be pathogenic to both plants and man, J2315 is representative of a lineage of B. cenocepacia rarely isolated from the environment and which spreads between CF patients. Comparative analysis revealed that ca. 21% of the genome is unique in comparison to other strains of B. cenocepacia, highlighting the genomic plasticity of this species. Pseudogenes in virulence determinants suggest that the pathogenic response of J2315 may have been recently selected to promote persistence in the CF lung. The J2315 genome contains evidence that its unique and highly adapted genetic content has played a significant role in its success as an epidemic CF pathogen.

U2 - 10.1128/JB.01230-08

DO - 10.1128/JB.01230-08

M3 - Journal article

C2 - 18931103

SN - 0021-9193

VL - 191

SP - 261

EP - 277

JO - Journal of Bacteriology

JF - Journal of Bacteriology

IS - 1

ER -

The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients

Abstract

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