Distribution of cepacian biosynthesis genes among environmental and clinical Burkholderia strains and role of cepacian exopolysaccharide in resistance to stress conditions

Applied and Environmental Microbiology

Volumn 76, Issue 2, 2010, Pages 441-450

  Ferreira, Ana S ^a   Leitão, Jorge H ^a   Silva, Inês N ^a   Pinheiros, Pedro F ^a   Sousa, Sílvia A ^a   Ramos, Christian G ^a   Moreira, Leonilde M ^a  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS GENES; BURKHOLDERIA; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA MULTIVORANS; CEPACIAN; CLINICAL ISOLATES; CYTOPLASMIC MEMBRANE; EPS PRODUCTION; EXOPOLYSACCHARIDES; GENE CLUSTERS; GENOME SEQUENCES; GLYCOSYL TRANSFERASE; NUCLEOTIDE SUGAR; PLANT GROWTH; REVERSE TRANSCRIPTION; STRESS CONDITION;

ACETYLATION; ANIMALS; BACTERIOLOGY; BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; COPOLYMERIZATION; ENCODING (SYMBOLS); FOURIER TRANSFORM INFRARED SPECTROSCOPY; GENE ENCODING; METAL IONS; PLANT LIFE EXTENSION; STRAIN; SUGAR (SUCROSE);

TRANSCRIPTION;

BACTERIAL POLYSACCHARIDE; CEPACIAN; METAL; POLYSACCHARIDE;

BACTERIUM; BIOREMEDIATION; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; FTIR SPECTROSCOPY; GENE; GENOME; MEMBRANE; POLYMERASE CHAIN REACTION; POLYSACCHARIDE; TRANSLOCATION;

ARTICLE; BIOSYNTHESIS; BURKHOLDERIA CEPACIA COMPLEX; GENETICS; INFRARED SPECTROSCOPY; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; VIRULENCE;

BASE SEQUENCE; BURKHOLDERIA CEPACIA COMPLEX; METALS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; POLYSACCHARIDES; POLYSACCHARIDES, BACTERIAL; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STRESS, PHYSIOLOGICAL; VIRULENCE;

ANIMALIA; BURKHOLDERIA; BURKHOLDERIA CEPACIA; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA MULTIVORANS;

EID: 75249087222     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01828-09     Document Type: Article

References (52)

1. Altschul, S. F., T. L. Madden, A. A Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Bartholdson, S. J, A. R. Brown, B. R. Mewburn, D. J. Clarke, S. C. Fry, D. J. Campopiano, and J. R. Govan. 2008. Plant host and sugar alcohol induced exopolysaccharide biosynthesis in the Burkholderia cepacia complex. Microbiology 154: 2513-2521.
3. Buendia, A. M., B. Enenkel, R. Koplin, K. Niehaus, W. Arnold, and A. Puhler. 1991. The Rhizobium melilotl exoZl exoB fragment of megaplasmid 2: ExoB functions as a UDP-glucose 4-epimerase and ExoZ shows homology to NodX of Rhizobium legumlnosarum biovar viciae strain TOM. Mol. Microbiol. 5: 1519-1530.
4. Bullock, W. C., J. M. Femandz, and J. M. Short. 1987. XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. Biotechniques 5: 376-379.
5. Bylund, J., L. A. Burgess, P. Cescutti, R. K. Ernst, and D. P. Speert. 2006. Exopolysaccharides from Burkholderia cenocepacla inhibit neutrophil Chemotaxis and scavenge reactive oxygen, species. J. Biol. Clem. 281: 2526-2532.
6. Cescutti, P., M. Bosco, F. Picotti, G. Impallomeni, J. H. Leitão, J. A. Richau, and I. Sá-Correia. 2000. Structural study of the exopolysaccharide produced by a clinical isolate of Burkholderia cepacia. Biochem. Biophys. Res. Commun. 273: 1088-1094.
7. Chiarini, L., P. Cescutti, L. Drigo, G. Impallomeni, Y. Herasimenka, A. Bevivino, C. Dalmastri, S. Tabacchioni, G. Manno, F. Zanetti, and R. Rizzo. 2004. Exopolysaccharides produced by Burkholderia cenocepacla recA lineages IIIA and IIIB. J. Cyst. Fibros. 3: 165-172.
8. Coenye, T., J. J. LiPuma, D. Henry, B. Hoste, K. Vandemeulebroecke, M. Gillis, D. P. Speert, and P. Vandamme. 2001. Burkholderia cepacia genomovar VI, a new member of the Burkholderia cepacia complex isolated from cystic fibrosis patients. Int. J. Syst. Evol. Microbiol. 51: 271-279.
9. Coenye, T., E. Mahenthiralingam, D. Henry, J. J. LiPuma, S. Laevens, M. Gillis, D. P. Speert, and P. Vandamme. 2001. Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int. J. Syst. Evol. Microbiol. 51: 1481-1490.
10. Conway, B. A., K. K. Chu, J. Bylund, E. Altman, and D. P. Speert. 2004. Production, of exopolysaccharide by Burkholderia cenocepacla results in altered cell-surface interactions and altered bacterial clearance in mice. J. Infect. Dis. 190: 957-966.
11. Cunha, M. V., S. A. Sousa, J. H. Leitão, L. M. Moreira, P. A. Videira, and I. Sá-Correia. 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.
12. Cuthbertson, L., I. L. Mainprize, J. H. Naismith, and C. Whitfield. 2009. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in gram-negative bacteria. Microbiol. MoI. Biol. Rev. 73: 155-177.
13. Denny, T. P. 1995. Involvement of bacterial polysaccharides in plant pathogenesis. Annu. Rev. Phytopathol. 33: 173-197.
14. Dudman, W. F. 1977. The role of surface polysaccharides in natural environments, p. 357-414. In. I. W. Sutherland (ed.), Surface carbohydrates of the prokaryotic cell. Academic Press, New York, NY.
15. Ferreira, A. S., J. H. Leitão, S. A. Sousa, A. M. Cosme, I. Sá-Correia, and L M. Moreira. 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.
16. Firmin, J. L., K. E. Wilson, R. W. Carlson, A. E. Davies, and J. A. Downie. 1993. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol. Microbiol. 10: 351-360.
17. Gibson, K. E., H. Kobayashi, and G. C. Walker. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42: 413-441.
18. Goris, J., P. De Vos, J. Caballero-Mellado, J. Park, E. Falsen, J. F. Quensen III, J. M. Tiedje, and P. Vandamme. 2004. Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400T and relatives as Burkholderia xenovorans sp. nov. Int. J. Syst. Evol. Microbiol. 54: 1677-1681.
19. Govan, J. R., P. H. Brown, J. Maddison, C. J. Doherty, J. W. Nelson, M. Dodd, A. P. Greening, and A. K. Webb. 1993. Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 342: 15-19.
20. Herasimenka, Y., P. Cescutti, G. Impallomeni, S. Campana, G. Taccetti, N. Ravenni, F. Zanetti, and R. Rizzo. 2007. Exopolysaccharides produced by clinical strains belonging to the Burkholderia cepacia complex. J. Cyst. Fibros. 6: 145-152.
21. Knowles, E. J., and R. W. Castenholz. 2008. Effect of exogenous extracellular polysaccharides on the desiccation and freezing tolerance of rock-inhabiting phototrophic microorganisms. FEMS Microbiol. Ecol. 66: 261-270.
22. Koch, C., and N. Holby. 1993. Pathogenesis of cystic fibrosis. Lancet 341: 1065-1069.
23. Komlos, J., A. B. Cunningham, A. K. Camper, and R. R. Sharp. 2005. Interaction of Klebsiella oxytoca and Burkholderia cepacia in dual-species batch cultures and biofilms as a. function of growth rate and substrate concentration. Microb. Ecol. 49: 114-125.
24. Kooistra, O., E. Luneberg, B. Lindner, Y. A. Knirel, M. Frosch, and U. Zahringer. 2001. Complex O-acetylation in Legionella pneumophila serogroup 1 lipopolysaccharide. Evidence for two genes involved in 8-O-acetylation of legionaminic acid. Biochemistry 40: 7630-7640.
25. Lefebre, M. D., and M. A Valvano. 2002. Construction, and evaluation of plasmid vectors optimized for constitutive and regulated gene expression in Burkholderia cepacia complex isolates. Appl. Environ. Microbiol. 68: 5956-5964.
26. Loutet, S. A., S. J. Bartholdson, J. R. Govan, D. J. Campopiano, and M. A. Valvano. 2009. Contributions of two UDP-glucose dehydrogenases to viability and polymyxin B resistance of Burkholderia cenocepacla. Microbiology 155: 2029-2039.
27. Mahenthiralingam, E., T. A. Urban, and J. B. Goldberg. 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3: 144-156.
28. Markowitz, V. M., E. Szeto, K. Palaniappan, Y. Grechkin, K. Chu, I. M. Chen, I. Dubchak, I. Anderson, A. Lykidis, K. Mavromatis, N. N. Ivanova, and N. C. Kyrpides. 2008. The integrated microbial genomes (IMG) system, in 2007: data content and analysis tool extensions. Nucleic Acids Res. 36: D528-D533.
29. Marolda, C. L., J. Vlcarioll, and M. A. Valvano. 2004. Wzx proteins involved in biosynthesis of O antigen function in association with the first sugar of the O-specific lipopolysaccharide subunit. Microbiology 150: 4095-4105.
30. McComb, E. A., and R. M. McCready. 1957. Determination of acetyl in pectin and acetylated carbohydrate polymers. Anal. Chem. 29: 819-821.
31. Moreira, L. M., P. A. Videira, S. A. Sousa, J. H. Leitão, M. V. Cunha, and I. Sá-Correia. 2003. Identification and physical organization of the gene duster involved in the biosynthesis of Burkholderia cepacia complex exopolysaccharide. Biochem. Biophys. Res. Commun. 312: 323-333.
32. Nelson, M. J, S. O. Montgomery, W. R. Mahaffey, and P. H. Prltchard. 1987. Biodegradation of trichloroethylene and involvement of an aromatic biodegradative pathway. Appl. Environ. Microbiol. 53: 949-954.
33. Park, K., J. W. Kloepper, and C. M. Ryu. 2008. Rhizobacterial exopolysaccharides elicit induced resistance on cucumber. J. Microbiol. Biotechnol. 18: 1095-1100.
34. Pfaffi, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
35. Pier, G. B., F. Coleman, M. Grout, M. Franklin, and D. E. Ohman. 2001. Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect. Immun. 69: 1895-1901.
36. Potts, M. 1994. Desiccation tolerance of prokaryotes. Microbiol. Rev. 58: 755-805.
37. Richau, J. A., J. H. Leitão, M. Correia, L. Lito, M. J. Salgado, C. Barreto, P. Cescutti, and I. Sá-Correla. 2000. Molecular typing and exopolysaccharide biosynthesis of Burkholderia cepacia isolates from a Portuguese cystic fibrosis center. J. Cilin. Microbiol. 38: 1651-1655.
38. Richau, J. A., J. H. Leitão, and I. Sá-Correia. 2000. Enzymes leading to the nucleotide sugar precursors for exopolysaccharide synthesis in Burkholderia cepacia. Biochem. Biophys. Res. Commun. 276: 71-76.
39. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual. CSHL Press, New York, NY.
40. Sessitsch, A., T. Coenye, A V. Sturz, P. Vandamme, E. A. Barka, J. F. Salles, J. D. Van Elsas, D. Faure, B. Reiter, B. R. Click, G. Wang-Pruski, and J. Nowak. 2005. Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int. J. Syst. Evol. Microbiol. 55: 1187-1192.
41. Slauch, J. M., A. A. Lee, M. J. Mahan, and J. J. Mekalanos. 1996. Molecular characterization of the oaf A locus responsible for acetylation of Salmonella typhimurium O-antigen: oafA is a member of a family of integral membrane trans-acylases. J. Bacteriol. 178: 5904-5909.
42. Sousa, S. A., L. M. Moreira, J. Wopperer, L. Eberl, I. Sá-Correia, and J. H. Leitão. 2007. The Burkholderia cepacia bceA gene encodes a protein with phosphomannose isomerase and GDP-D-mannose pyrophosphorylase activities. Biochem. Biophys. Res. Commun. 353: 200-206.
43. phox-/- mice. Cell. Microbiol. 9: 2817-2825.
44. Stanier, R. Y., N. J. Palleroni, and M. Doudoroff. 1966. The aerobic pseudomonads: a taxonomie study. J. Gen. Microbiol. 43: 159-271.
45. 45. Tamaru, Y., Y. Takani, T. Yoshida, and T. Sakamoto. 2005. Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol. 71: 7327-7333. (Pubitemid 43194228)
46. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CXUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
47. Vandamme, P., J. Goris, W. M. Chen, P. de Vos, and A. Willems. 2002. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst. Appl. Microbiol. 25: 507-512.
48. Vandamme, P., B. Holmes, M. Vancanneyt, T. Coenye, B. Hoste, R. Coopman, H. Revets, S. Lauwers, M. Gillis, K. Kersters, and J. R. Govan. 1997. Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multlvorans sp. nov. Int. J. Syst. Bacteriol. 47: 1188-1200.
49. Vanlaere, E., A. Baldwin, D. Gevers, D. Henry, E. De Brandt, J. J. LiPuma, E. Mahenthiralingam, D. P. Speert, C. Dowson, and P. Vandamme. 2009. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contamlnans sp. nov. and Burkholderia lata sp. nov. Int. J. Syst. Evol. Microbiol. 59: 102-111.
50. Videira, P. A., A. P. Garcia, and I. Sá-Correia. 2005. Functional and topological analysis of the Burkholderia cenocepacla priming glucosyltransferase BceB, involved in the biosynthesis of the cepacian exopolysaccharide. J. Bacteriol. 187: 5013-5018.
51. Vriezen, J. A., F. J. de Bruijn, and K. Nusslein. 2006. Desiccation responses and survival of Sinorhizobium melllotl USDA 1021 in relation to growth phase, temperature, chloride and sulfate availability. Lett. Appl. Microbiol. 42: 172-178.
52. Zlosnik, J. E., T. J. Hird, M. C. Fraenkel, L. M. Moreira, D. A Henry, and D. P. Speert. 2008. Differential mucoid exopolysaccharide production, by members of the Burkholderia cepacia complex. J. Clin. Microbiol. 46: 1470-1473.