Plant host and sugar alcohol induced exopolysaccharide biosynthesis in the Burkholderia cepacia complex

• Published in: Microbiology (Society for General Microbiology) Vol. 154; no. 8; pp. 2513 - 2521
• Main Authors: Bartholdson, S. Josefin, Brown, Alan R, Mewburn, Ben R, Clarke, David J, Fry, Stephen C, Campopiano, Dominic J, Govan, John R. W
• Format: Journal Article
• Language: English
• Published: Reading Soc General Microbiol 01-08-2008; Society for General Microbiology
• Subjects: Allium cepa; Bacteriology; Biological and medical sciences; Burkholderia cepacia; Burkholderia cepacia complex - genetics; Burkholderia cepacia complex - metabolism; Carbohydrate Metabolism; Fundamental and applied biological sciences. Psychology; Microbiology; Onions - chemistry; Onions - metabolism; Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains; Plant Extracts - chemistry; Plant Extracts - metabolism; Polysaccharides, Bacterial - biosynthesis; Polysaccharides, Bacterial - genetics; Sugar Alcohols - metabolism; Allium cepa; Polysaccharide-lyases; Monocotyledones; Enzyme; Alcohol; Lyases; Biosynthesis; Chromatography; Infection; Melioidosis; Liliaceae; Plant; Vegetable crop; Burkholderia cepacia; Angiospermae; Bacteriosis; Bacteria; Spermatophyta; Carbon-oxygen lyases; Reverse transcription polymerase chain reaction; Sugar
• ISSN: 1350-0872; 1465-2080
• DOI: 10.1099/mic.0.2008/019216-0

1 School of Chemistry, University of Edinburgh, Edinburgh EH9 3JJ, UK
2 Centre for Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK
3 Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3JH, UK
Correspondence John R. W. Govan john.r.w.govan{at}ed.ac.uk
The species that presently constitute the Burkholderia cepacia complex (Bcc) have multiple roles; they include soil and water saprophytes, bioremediators, and plant, animal and human pathogens. Since the first description of pathogenicity in the Bcc was based on sour skin rot of onion bulbs, this study returned to this plant host to investigate the onion-associated phenotype of the Bcc. Many Bcc isolates, which were previously considered to be non-mucoid, produced copious amounts of exopolysaccharide (EPS) when onion tissue was provided as the sole nutrient. EPS production was not species-specific, was observed in isolates from both clinical and environmental sources, and did not correlate with the ability to cause maceration of onion tissue. Chemical analysis suggested that the onion components responsible for EPS induction were primarily the carbohydrates sucrose, fructose and fructans. Additional sugars were investigated, and all alcohol sugars tested were able to induce EPS production, in particular mannitol and glucitol. To investigate the molecular basis for EPS biosynthesis, we focused on the highly conserved bce gene cluster thought to be involved in cepacian biosynthesis. We demonstrated induction of the bce gene cluster by mannitol, and found a clear correlation between the inability of representatives of the Burkholderia cenocepacia ET12 lineage to produce EPS and the presence of an 11 bp deletion within the bceB gene, which encodes a glycosyltransferase. Insertional inactivation of bceB in Burkholderia ambifaria AMMD results in loss of EPS production on sugar alcohol media. These novel and surprising insights into EPS biosynthesis highlight the metabolic potential of the Bcc and show that a potential virulence factor may not be detected by routine laboratory culture. Our results also highlight a potential hazard in the use of inhaled mannitol as an osmolyte to improve mucociliary clearance in individuals with cystic fibrosis.
Abbreviations: Bcc, Burkholderia cepacia complex; CF, cystic fibrosis; CGD, chronic granulomatous disease; EPS, exopolysaccharide; HPAE-PAD, high-performance anion-exchange chromatography with pulsed amperometric detection; TFA, trifluoroacetic acid
Three supplementary tables and a supplementary figure are available with the online version of this paper.
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