Growth on mannitol-rich media elicits a genomewide transcriptional response in Burkholderia multivorans that impacts on multiple virulence traits in an exopolysaccharide-independent manner

Microbiology (United Kingdom)

Volumn 160, Issue PART 1, 2014, Pages 187-197

  Denman, Carmen C ^a,c   Robinson, Matthew T ^a   Sass, Andrea M ^b,d   Mahenthiralingam, Eshwar ^b   Brown, Alan R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; MANNITOL; PHOSPHOLIPASE;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOFILM; BURKHOLDERIA MULTIVORANS; CELL INVASION; CONTROLLED STUDY; CYSTIC FIBROSIS; EPITHELIUM CELL; FLAGELLUM; GENE CLUSTER; GENE SEQUENCE; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; UPREGULATION; YEAST;

ANIMALS; BIOFILMS; BURKHOLDERIA CEPACIA COMPLEX; CELL LINE; CULTURE MEDIA; ENDOCYTOSIS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LEPIDOPTERA; LOCOMOTION; MANNITOL; POLYSACCHARIDES, BACTERIAL; SURVIVAL ANALYSIS; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

EID: 84891589296     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.072975-0     Document Type: Article

References (67)

1. Allenza, P., Lee, Y. N. & Lessie, T. G. (1982). Enzymes related to fructose utilization in Pseudomonas cepacia. J Bacteriol 150, 1348-1356.
2. Allenza, P., Morrell, M. J. & Detroy, R. W. (1990). Conversion of mannose to fructose by immobilized mannose isomerase from Pseudomonas cepacia. Appl Biochem Biotechnol 24-25, 171-182.
3. Allison, K. R., Brynildsen, M. P. & Collins, J. J. (2011). Metaboliteenabled eradication of bacterial persisters by aminoglycosides. Nature 473, 216-220.
4. Baran, D., de Vuyst, P. & Ooms, H. A. (1990). Concentration of tobramycin given by aerosol in the fluid obtained by bronchoalveolar lavage. Respir Med 84, 203-204.
5. Bartholdson, S. J., Brown, A. R., Mewburn, B. R., Clarke, D. J., Fry, S. C., Campopiano, D. J. & Govan, J. R. (2008). Plant host and sugar alcohol induced exopolysaccharide biosynthesis in the Burkholderia cepacia complex. Microbiology 154, 2513-2521.
6. Bilton, D., Robinson, P., Cooper, P., Gallagher, C. G., Kolbe, J., Fox, H., Jaques, A., Charlton, B. & CF301 Study Investigators (2011). Inhaled dry powder mannitol in cystic fibrosis: an efficacy and safety study. Eur Respir J 38, 1071-1080.
7. Brünker, P., Altenbuchner, J. & Mattes, R. (1998). Structure and function of the genes involved in mannitol, arabitol and glucitol utilization from Pseudomonas fluorescens DSM50106. Gene 206, 117-126.
8. Bucior, I., Abbott, J., Song, Y., Matthay, M. A. & Engel, J. N. (2013). Sugar administration is an effective adjunctive therapy in the treatment of Pseudomonas aeruginosa pneumonia. Am J Physiol Lung Cell Mol Physiol 305, L352-L363.
9. Burns, J. L., Jonas, M., Chi, E. Y., Clark, D. K., Berger, A. & Griffith, A. (1996). Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 64, 4054-4059.
10. Bylund, J., Burgess, L. A., Cescutti, P., Ernst, R. K. & Speert, D. P. (2006). Exopolysaccharides from Burkholderia cenocepacia inhibit neutrophil chemotaxis and scavenge reactive oxygen species. J Biol Chem 281, 2526-2532.
11. Conway, B. A., Chu, K. K., Bylund, J., Altman, E. & Speert, D. P. (2004). Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell-surface interactions and altered bacterial clearance in mice. J Infect Dis 190, 957-966.
12. Courtney, J. M., Dunbar, K. E., McDowell, A., Moore, J. E., Warke, T. J., Stevenson, M. & Elborn, J. S. (2004). Clinical outcome of Burkholderia cepacia complex infection in cystic fibrosis adults. J Cyst Fibros 3, 93-98.
13. Cunha, M. V., Sousa, S. A., Leitão, J. H., Moreira, L. M., Videira, P. A. & Sá-Correia, I. (2004). Studies on the involvement of the exopolysaccharide produced by cystic fibrosis-associated isolates of the Burkholderia cepacia complex in biofilm formation and in persistence of respiratory infections. J Clin Microbiol 42, 3052-3058.
14. Daviskas, E., Anderson, S. D., Jaques, A. & Charlton, B. (2010). Inhaled mannitol improves the hydration and surface properties of sputum in patients with cystic fibrosis. Chest 137, 861-868.
15. Denman, C. C. & Brown, A. R. (2013). Mannitol promotes adherence of an outbreak strain of Burkholderia multivorans via an exopolysaccharide-independent mechanism that is associated with upregulation of newly identified fimbrial and afimbrial adhesins. Microbiology 159, 771-781.
16. Dubois, M., Gilles, K., Hamilton, J. K., Rebers, P. A. & Smith, F. (1951). A colorimetric method for the determination of sugars. Nature 168, 167.
17. Etherington, C., Peckham, D. G., Conway, S. P. & Denton, M. (2003). Burkholderia cepacia complex infection in adult patients with cystic fibrosis-is early eradication possible? J Cyst Fibros 2, 220-221.
18. Ferreira, A. S., Leitão, J. H., Sousa, S. A., Cosme, A. M., Sá-Correia, I. & Moreira, L. M. (2007). Functional analysis of Burkholderia cepacia genes bceD and bceF, encoding a phosphotyrosine phosphatase and a tyrosine autokinase, respectively: role in exopolysaccharide biosynthesis and biofilm formation. Appl Environ Microbiol 73, 524-534.
19. Ferreira, A. S., Leitão, J. H., Silva, I. N., Pinheiro, P. F., Sousa, S. A., Ramos, C. G. & Moreira, L. M. (2010). Distribution of cepacian biosynthesis genes among environmental and clinical Burkholderia strains and role of cepacian exopolysaccharide in resistance to stress conditions. Appl Environ Microbiol 76, 441-450.
20. Ferreira, A. S., Silva, I. N., Oliveira, V. H., Becker, J. D., Givskov, M., Ryan, R. P., Fernandes, F. & Moreira, L. M. (2013). Comparative transcriptomic analysis of the Burkholderia cepacia tyrosine kinase bceF mutant reveals a role in tolerance to stress, biofilm formation, and virulence. Appl Environ Microbiol 79, 3009-3020.
21. Flannagan, R. S., Aubert, D., Kooi, C., Sokol, P. A. & Valvano, M. A. (2007). Burkholderia cenocepacia requires a periplasmic HtrA protease for growth under thermal and osmotic stress and for survival in vivo. Infect Immun 75, 1679-1689.
22. Gotschlich, A., Huber, B., Geisenberger, O., Tögl, A., Steidle, A., Riedel, K., Hill, P., Tümmler, B., Vandamme, P. & other authors (2001). Synthesis of multiple N-acylhomoserine lactones is widespread among the members of the Burkholderia cepacia complex. Syst Appl Microbiol 24, 1-14.
23. Govan, J. R., Brown, A. R. & Jones, A. M. (2007). Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol 2, 153-164.
24. Graindorge, A., Menard, A., Neto, M., Bouvet, C., Miollan, R., Gaillard, S., de Montclos, H., Laurent, F. & Cournoyer, B. (2010). Epidemiology and molecular characterization of a clone of Burkholderia cenocepacia responsible for nosocomial pulmonary tract infections in a French intensive care unit. Diagn Microbiol Infect Dis 66, 29-40.
25. Hamad, M. A., Skeldon, A. M. & Valvano, M. A. (2010). Construction of aminoglycoside-sensitive Burkholderia cenocepacia strains for use in studies of intracellular bacteria with the gentamicin protection assay. Appl Environ Microbiol 76, 3170-3176.
26. Hanulik, V., Webber, M. A., Chroma, M., Uvizl, R., Holy, O., Whitehead, R. N., Baugh, S., Matouskova, I. & Kolar, M. (2013). An outbreak of Burkholderia multivorans beyond cystic fibrosis patients. J Hosp Infect 84, 248-251.
27. Herasimenka, Y., Cescutti, P., Impallomeni, G., Campana, S., Taccetti, G., Ravenni, N., Zanetti, F. & Rizzo, R. (2007). Exopolysaccharides produced by clinical strains belonging to the Burkholderia cepacia complex. J Cyst Fibros 6, 145-152.
28. Isles, A., Maclusky, I., Corey, M., Gold, R., Prober, C., Fleming, P. & Levison, H. (1984). Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104, 206-210.
29. Jaques, A., Daviskas, E., Turton, J. A., McKay, K., Cooper, P., Stirling, R. G., Robertson, C. F., Bye, P. T., Lesouëf, P. N. & other authors (2008). Inhaled mannitol improves lung function in cystic fibrosis. Chest 133, 1388-1396.
30. Jones, A. M., Dodd, M. E., Govan, J. R., Barcus, V., Doherty, C. J., Morris, J. & Webb, A. K. (2004). Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis. Thorax 59, 948-951.
31. Kalish, L. A., Waltz, D. A., Dovey, M., Potter-Bynoe, G., McAdam, A. J., LiPuma, J. J., Gerard, C. & Goldmann, D. (2006). Impact of Burkholderia dolosa on lung function and survival in cystic fibrosis. Am J Respir Crit Care Med 173, 421-425.
32. Keith, K. E. & Valvano, M. A. (2007). Characterization of SodC, a periplasmic superoxide dismutase from Burkholderia cenocepacia. Infect Immun 75, 2451-2460.
33. Keith, K. E., Killip, L., He, P., Moran, G. R. & Valvano, M. A. (2007). Burkholderia cenocepacia C5424 produces a pigment with antioxidant properties using a homogentisate intermediate. J Bacteriol 189, 9057-9065.
34. Korbsrisate, S., Tomaras, A. P., Damnin, S., Ckumdee, J., Srinon, V., Lengwehasatit, I., Vasil, M. L. & Suparak, S. (2007). Characterization of two distinct phospholipase C enzymes from Burkholderia pseudomallei. Microbiology 153, 1907-1915.
35. Law, R. J., Hamlin, J. N., Sivro, A., McCorrister, S. J., Cardama, G. A. & Cardona, S. T. (2008). A functional phenylacetic acid catabolic pathway is required for full pathogenicity of Burkholderia cenocepacia in the Caenorhabditis elegans host model. J Bacteriol 190, 7209-7218.
36. Lefebre, M. & Valvano, M. (2001). In vitro resistance of Burkholderia cepacia complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production. Microbiology 147, 97-109.
37. Lewenza, S., Conway, B., Greenberg, E. P. & Sokol, P. A. (1999). Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181, 748-756.
38. Liou, T. G., Adler, F. R., Fitzsimmons, S. C., Cahill, B. C., Hibbs, J. R. & Marshall, B. C. (2001). Predictive 5-year survivorship model of cystic fibrosis. Am J Epidemiol 153, 345-352.
39. LiPuma, J. J. (2010). The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23, 299-323.
40. Mahenthiralingam, E., Coenye, T., Chung, J. W., Speert, D. P., Govan, J. R., Taylor, P. & Vandamme, P. (2000). Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38, 910-913.
41. Mann, T., Ben-David, D., Zlotkin, A., Shachar, D., Keller, N., Toren, A., Nagler, A., Smollan, G., Barzilai, A. & Rahav, G. (2010). An outbreak of Burkholderia cenocepacia bacteremia in immunocompromised oncology patients. Infection 38, 187-194.
42. Messiaen, A. S., Nelis, H. & Coenye, T. (2013). Investigating the role of matrix components in protection of Burkholderia cepacia complex biofilms against tobramycin. J Cyst Fibros.
43. Middleton, P. G., Kidd, T. J. & Williams, B. (2005). Combination aerosol therapy to treat Burkholderia cepacia complex. Eur Respir J 26, 305-308.
44. Moore, R. A., DeShazer, D., Reckseidler, S., Weissman, A. & Woods, D. E. (1999). Efflux-mediated aminoglycoside and macrolide resistance in Burkholderia pseudomallei. Antimicrob Agents Chemother 43, 465-470.
45. Moreira, L. M., Videira, P. A., Sousa, S. A., Leitão, J. H., Cunha, M. V. & Sá-Correia, I. (2003). Identification and physical organization of the gene cluster involved in the biosynthesis of Burkholderia cepacia complex exopolysaccharide. Biochem Biophys Res Commun 312, 323-333.
46. Palmer, K. L., Aye, L. M. & Whiteley, M. (2007). Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol 189, 8079-8087.
47. Rose, H., Baldwin, A., Dowson, C. G. & Mahenthiralingam, E. (2009). Biocide susceptibility of the Burkholderia cepacia complex. J Antimicrob Chemother 63, 502-510.
48. Sage, A., Linker, A., Evans, L. R. & Lessie, T. G. (1990). Hexose phosphate metabolism and exopolysaccharide formation in Pseudomonas cepacia. Curr Microbiol 20, 191-198.
49. Sass, A., Marchbank, A., Tullis, E., LiPuma, J. J. & Mahenthiralingam, E. (2011). Spontaneous and evolutionary changes in the antibiotic resistance of Burkholderia cenocepacia observed by global gene expression analysis. BMC Genomics 12, 373.
50. Sass, A. M., Schmerk, C., Agnoli, K., Norville, P. J., Eberl, L., Valvano, M. A. & Mahenthiralingam, E. (2013). The unexpected discovery of a novel low-oxygen-activated locus for the anoxic persistence of Burkholderia cenocepacia. ISME J 7, 1568-1581.
51. Schmerk, C. L. & Valvano, M. A. (2013). Burkholderia multivorans survival and trafficking within macrophages. J MedMicrobiol 62, 173-184.
52. Shafiq, I., Carroll, M. P., Nightingale, J. A. & Daniels, T. V. (2011). Cepacia syndrome in a cystic fibrosis patient colonised with Burkholderia multivorans. BMJ Case Rep 2011, doi: 10. 1136/bcr. 08. 2010. 3296.
53. Sokol, P. A., Darling, P., Woods, D. E., Mahenthiralingam, E. & Kooi, C. (1999). Role of ornibactin biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the gene encoding Lornithine N (5)-oxygenase. Infect Immun 67, 4443-4455.
54. Sokol, P. A., Darling, P., Lewenza, S., Corbett, C. R. & Kooi, C. D. (2000). Identification of a siderophore receptor required for ferric ornibactin uptake in Burkholderia cepacia. Infect Immun 68, 6554-6560.
55. Subsin, B., Chambers, C. E., Visser, M. B. & Sokol, P. A. (2007). Identification of genes regulated by the cepIR quorum-sensing system in Burkholderia cenocepacia by high-throughput screening of a random promoter library. J Bacteriol 189, 968-979.
56. Tatusov, R. L., Galperin, M. Y., Natale, D. A. & Koonin, E. V. (2000). The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28, 33-36.
57. Teper, A., Jaques, A. & Charlton, B. (2011). Inhaled mannitol in patients with cystic fibrosis: A randomised open-label dose response trial. J Cyst Fibros 10, 1-8.
58. Tomich, M., Herfst, C. A., Golden, J. W. & Mohr, C. D. (2002). Role of flagella in host cell invasion by Burkholderia cepacia. Infect Immun 70, 1799-1806.
59. Tseng, B. S., Zhang, W., Harrison, J. J., Quach, T. P., Song, J. L., Penterman, J., Singh, P. K., Chopp, D. L., Packman, A. I. & Parsek, M. R. (2013). The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ Microbiol 15, 2865-2878.
60. Tunpiboonsak, S., Mongkolrob, R., Kitudomsub, K., Thanwatanaying, P., Kiettipirodom, W., Tungboontina, Y. & Tungpradabkul, S. (2010). Role of a Burkholderia pseudomallei polyphosphate kinase in an oxidative stress response, motilities, and biofilm formation. J Microbiol 48, 63-70.
61. Urban, T. A., Griffith, A., Torok, A. M., Smolkin, M. E., Burns, J. L. & Goldberg, J. B. (2004). Contribution of Burkholderia cenocepacia flagella to infectivity and inflammation. Infect Immun 72, 5126-5134.
62. Vial, L., Chapalain, A., Groleau, M. C. & Déziel, E. (2011). The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ Microbiol 13, 1-12.
63. Whiteford, M. L., Wilkinson, J. D., McColl, J. H., Conlon, F. M., Michie, J. R., Evans, T. J. & Paton, J. Y. (1995). Outcome of Burkholderia (Pseudomonas) cepacia colonisation in children with cystic fibrosis following a hospital outbreak. Thorax 50, 1194-1198.
64. Winsor, G. L., Khaira, B., Van Rossum, T., Lo, R., Whiteside, M. D. & Brinkman, F. S. (2008). The Burkholderia Genome Database: facilitating flexible queries and comparative analyses. Bioinformatics 24, 2803-2804.
65. Woods, C. W., Bressler, A. M., LiPuma, J. J., Alexander, B. D., Clements, D. A., Weber, D. J., Moore, C. M., Reller, L. B. & Kaye, K. S. (2004). Virulence associated with outbreak-related strains of Burkholderia cepacia complex among a cohort of patients with bacteremia. Clin Infect Dis 38, 1243-1250.
66. Zahariadis, G., Levy, M. H. & Burns, J. L. (2003). Cepacia-like syndrome caused by Burkholderia multivorans. Can J Infect Dis Med Microbiol 14, 123-125.
67. Zlosnik, J. E., Costa, P. S., Brant, R., Mori, P. Y., Hird, T. J., Fraenkel, M. C., Wilcox, P. G., Davidson, A. G. & Speert, D. P. (2011). Mucoid and nonmucoid Burkholderia cepacia complex bacteria in cystic fibrosis infections. Am J Respir Crit Care Med 183, 67-72.