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The multifarious, multireplicon Burkholderia cepacia complex

Nature Reviews Microbiology volume 3, pages 144–156 (2005)Cite this article

Key Points

  • Members of the Burkholderia cepacia complex (Bcc) can cause disease or can be beneficial for plants. The Bcc bacteria are nutritionally diverse and can grow in diverse environments; some can even degrade important pollutants or can use penicillin G as a sole source of carbon.

  • Bcc bacteria can act as opportunistic pathogens and are associated with a variable clinical course in patients with cystic fibrosis (CF) that can include severe lung infections, necrotizing pneumonia and septicaemia.

  • The Bcc currently includes nine species (genomovars). The most common species that cause infections in CF patients are B. cenocepacia (genomovar III) and B. multivorans (genomovar II).

  • Epidemiological studies have identified highly transmissible clones of Bcc bacteria, some of which have been associated with serious outbreaks among CF patients. One of the most prevalent belongs to the ET-12 lineage.

  • However, the factors responsible for the transmission and virulence of these or other epidemic strains have not been identified. It is suggested that, in addition to bacterial factors, the host response is responsible for the variable clinical course among patients.

  • The availability of genome sequence data for the ET-12 lineage strain B. cenocepacia J2315 has led to the identification of novel genomic islands and facilitated the development of genetic tools to investigate the pathogenesis of this bacterium.

  • These tools have been exploited, along with various models systems that include infections in cell cultures, animals, plants, worms, and amoebae, which have led to the identification and characterization of potential virulence factors.

Abstract

The Burkholderia cepacia complex (Bcc) is a collection of genetically distinct but phenotypically similar bacteria that are divided into at least nine species. Bcc bacteria are found throughout the environment, where they can have both beneficial and detrimental effects on plants and some members can also degrade natural and man-made pollutants. Bcc bacteria are now recognized as important opportunistic pathogens that can cause variable lung infections in cystic fibrosis patients, which result in asymptomatic carriage, chronic infection or 'cepacia syndrome', which is characterized by a rapid decline in lung function that can include invasive disease. Here we highlight the unique characteristics of the Bcc, focusing on the factors that determine virulence.

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Figure 1: Beneficial and detrimental effects of the Burkholderia cepacia complex.
Figure 2: Genomic structure and major virulence factors of Burkholderia cenocepacia ET-12.
Figure 3: Structure of Burkholderia cepacia complex lipopolysaccharide and antibiotic-resistance mechanisms.

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Acknowledgements

T.A.U. and J.B.G. were supported by grants from the National Institutes of Health and the Cystic Fibrosis Foundation. E.M. acknowledges funding from the Cystic Fibrosis Trust, the Natural Environment Research Council and the Wellcome Trust. We apologize to our colleagues whose work was not cited owing to space considerations and acknowledge the inspiration provided by our collaborators in the International B. cepacia Working Group.

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Authors and Affiliations

  1. Cardiff School of Biosciences, Cardiff University, Cardiff, CF10 3TL, UK

    Eshwar Mahenthiralingam

  2. Department of Microbiology, University of Virginia, Charlottesville, 22908, Virginia, USA

    Teresa A. Urban & Joanna B. Goldberg

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  1. Eshwar Mahenthiralingam
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Correspondence to Joanna B. Goldberg.

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DATABASES

Entrez

Burkholderia SAR-1

B. cenocepacia strain J2315

FURTHER INFORMATION

Joanna B. Goldberg's laboratory

Eshwar Mahenthiralingam's laboratory

B. cenocepacia J2315 genome sequence

Cystic fibrosis

Environmental Protection Agency

International B. cepacia Working group

JGI Burkholderia genome sequences

United Kingdom CF Trust

Glossary

CYSTIC FIBROSIS

A disease caused by mutation of the cystic fibrosis transmembrane conductance regulator (CFTR). It presents with lung damage, gastrointestinal blockage and pancreatic insufficiency. Bacterial lung infections are the main cause of death.

MULTILOCUS ENZYME ELECTROPHORESIS

A strain typing method that examines the mobility of patterns of specific enzymes to derive phenotypic fingerprint of a given strain.

RANDOM AMPLIFIED POLYMORPHIC DNA ANALYSIS

A strain typing method that uses PCR to amplify random DNA markers from a bacterium and that generates a genetic fingerprint for a given strain.

PULSED FIELD GEL ELECTROPHORESIS

A method for the separation of large fragments of DNA that is applied in molecular epidemiology to visualize bacterial strain-specific genome fingerprints generated by restriction digestion of whole genomes.

REPETITIVE ELEMENT PCR

A strain typing method that uses PCR with primers directed against known short repetitive sequences that occur in bacterial DNA to derive a strain specific genetic fingerprint.

NECROTIZING PNEUMONIA

A lung infection that causes physical damage to pulmonary tissue.

SEPTICAEMIA

Bacterial infection that results from the spread of a pathogen into the bloodstream.

METAGENOMIC SEQUENCE

The entire genomic sequence of an organism, which is assembled from nucleotide sequence analysis of random DNA fragments that are isolated from the environment.

INSERTION SEQUENCES

Small transposable mobile DNA elements that are found in bacteria.

GENOMIC ISLANDS

Regions of genomic sequence that have unusual features, such as altered GC content, compared with most of the genome, indicating that they have been recently acquired during the evolution of a bacterial species.

RESTRICTION FRAGMENT LENGTH POLYMORPHISM

Sequence variation in a gene or stretch of DNA revealed by digestion with restriction enzymes and examination of the sizes of the digestion products.

SWARMING MOTILITY

The type of motility used by bacteria that move over a solid surface.

INTERMEDIATE FILAMENTS

Proteins that structure the cytoskeleton of the cell cytoplasm by forming very stable filaments that allow cells to resist external stress.

SIGNATURE-TAGGED MUTAGENESIS

Transposon mutagenesis in which each individual transposon mutant is tagged with a unique oligonucleotide that enables identification of a mutant by hybridization or PCR, even if the mutant is lost during an experimental screen.

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Mahenthiralingam, E., Urban, T. & Goldberg, J. The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3, 144–156 (2005). https://doi.org/10.1038/nrmicro1085

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