Phase variation has a role in Burkholderia ambifaria niche adaptation

ISME Journal

Volumn 4, Issue 1, 2010, Pages 49-60

  Vial, Ludovic ^a   Groleau, Marie Christine ^a   Lamarche, Martin G ^a   Filion, Geneviève ^b   Castonguay Vanier, Josée ^a   Dekimpe, Valérie ^a   Daigle, France ^c   Charette, Steve J ^b,d   Déziel, Eric ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

Opportunistic pathogen; Phase variation; Rhizosphere

Indexed keywords

VIRULENCE FACTOR;

ADAPTATION; ANIMAL; ARTICLE; BIOSYNTHESIS; BURKHOLDERIA CEPACIA COMPLEX; CELL CULTURE; DICTYOSTELIUM; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GROWTH, DEVELOPMENT AND AGING; HUMAN; LEPIDOPTERA; MACROPHAGE; MICROBIOLOGY; MONOCYTE; PATHOGENICITY; PHYSIOLOGY; PLANT ROOT; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BURKHOLDERIA CEPACIA COMPLEX; CELLS, CULTURED; DICTYOSTELIUM; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VARIATION; HUMANS; LEPIDOPTERA; MACROPHAGES; MONOCYTES; PLANT ROOTS; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA AMBIFARIA; BURKHOLDERIA CEPACIA COMPLEX; DICTYOSTELIUM DISCOIDEUM; DROSOPHILA MELANOGASTER; GALLERIA MELLONELLA;

EID: 73449133340     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2009.95     Document Type: Article

References (51)

1. Apicella MA, Griffiss JM, Schneider H. (1994). Isolation and characterization of lipopolysaccharides, lipooligosaccharides, and lipid A. Methods Enzymol 235: 242-252.
2. Aubert DF, Flannagan RS, Valvano MA. (2008). A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76: 1979-1991.
3. Bartholdson SJ, Brown AR, Mewburn BR, Clarke DJ, Fry SC, Campopiano DJ et al. (2008). Plant host and sugar alcohol induced exopolysaccharide biosynthesis in the Burkholderia cepacia complex. Microbiology 154: 2513-2521.
4. Bernier SP, Nguyen DT, Sokol PA. (2008). A LysR-type transcriptional regulator in Burkholderia cenocepacia influences colony morphology and virulence. Infect Immun 76: 38-47.
5. Bernier SP, Silo-Suh L, Woods DE, Ohman DE, Sokol PA. (2003). Comparative analysis of plant and animal models for characterization of Burkholderia cepacia virulence. Infect Immun 71: 5306-5313.
6. Brzostek A, Dziadek B, Rumijowska-Galewicz A, Pawelczyk J, Dziadek J. (2007). Cholesterol oxidase is required for virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett 275: 106-112.
7. Cardona ST, Wopperer J, Eberl L, Valvano MA. (2005). Diverse pathogenicity of Burkholderia cepacia complex strains in the Caenorhabditis elegans host model. FEMS Microbiol Lett 250: 97-104.
8. Chiarini L, Bevivino A, Dalmastri C, Tabacchioni S, Visca P. (2006). Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol 14: 277-286.
9. Coenye T, Mahenthiralingam E, Henry D, LiPuma JJ, Laevens S, Gillis M et al. (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. Compant S, Nowak J, Coenye T, Clement C, Ait Barka E. (2008). Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32: 607-626.
11. Cornillon S, Pech E, Benghezal M, Ravanel K, Gaynor E, Letourneur F et al. (2000). Phg1p is a nine-transmembrane protein superfamily member involved in Dictyostelium adhesion and phagocytosis. J Biol Chem 275: 34287-34292.
12. Déziel E, Comeau Y, Villemur R. (2001). Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183: 1195-1204.
13. Doukyu N, Aono R. (2001). Cloning, sequence analysis and expression of a gene encoding an organic solventand detergent-tolerant cholesterol oxidase of Burkholderia cepacia strain ST-200. Appl Microbiol Biotechnol 57: 146-152.
14. Dubern JF, Diggle SP. (2008). Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol Biosyst 4: 882-888.
15. Esselmann MT, Liu PV. (1961). Lecithinase production by gram-negative bacteria. J Bacteriol 81: 939-945.
16. Fahraeus G. (1957). The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16: 374-381.
17. Forest C, Faucher SP, Poirier K, Houle S, Dozois CM, Daigle F. (2007). Contribution of the stg fimbrial operon of Salmonella enterica serovar Typhi during interaction with human cells. Infect Immun 75: 5264-5271.
18. Govan JR, Brown AR, Jones AM. (2007). Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol 2: 153-164.
19. Govan JRW, Balendreau J, Vandamme P. (2000). Burkholderia cepacia-friend and foe. ASM News 66: 124-125.
20. Kooi C, Subsin B, Chen R, Pohorelic B, Sokol PA. (2006). Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect Immun 74: 4083-4093.
21. Lépine F, Déziel E, Milot S, Rahme LG. (2003). A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures. Biochim Biophys Acta 1622: 36-41.
22. LiPuma JJ, Spilker T, Coenye T, Gonzalez CF. (2002). An epidemic Burkholderia cepacia complex strain identified in soil. Lancet 359: 2002-2003.
23. Loutet SA, Flannagan RS, Kooi C, Sokol PA, Valvano MA. (2006). A complete lipopolysaccharide inner core oligosaccharide is required for resistance of Burkholderia cenocepacia to antimicrobial peptides and bacterial survival in vivo. J Bacteriol 188: 2073-2080.
24. Mahenthiralingam E, Urban TA, Goldberg JB. (2005). The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156. (Pubitemid 40207595)
25. Marolda CL, Hauroder B, John MA, Michel R, Valvano MA. (1999). Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145 (Pt 7): 1509-1517.
26. Martinez-Granero F, Rivilla R, Martin M. (2006). Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl Environ Microbiol 72: 3429-3434.
27. Mercanti V, Charette SJ, Bennett N, Ryckewaert JJ, Letourneur F, Cosson P. (2006). Selective membrane exclusion in phagocytic and macropinocytic cups. J Cell Sci 119: 4079-4087.
28. O'Sullivan LA, Weightman AJ, Jones TH, Marchbank AM, Tiedje JM, Mahenthiralingam E. (2007). Identifying the genetic basis of ecologically and biotechnologically useful functions of the bacterium Burkholderia vietnamiensis. Environ Microbiol 9: 1017-1034.
29. Parke JL, Gurian-Sherman D. (2001). Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39: 225-258.
30. Parke JL, Rand RE, Joy AE, King EB. (1991). Biological control of Aphanomyces root rot and Pythium damping-off of peas by application of Pseudomonas cepacia or Pseudomonas fluorescens applied to seed. Plant Dis 75: 987-992.
31. Payne GW, Vandamme P, Morgan SH, Lipuma JJ, Coenye T, Weightman AJ et al. (2005). Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl Environ Microbiol 71: 3917-3927.
32. Pearson JP, Pesci EC, Iglewski BH. (1997). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179: 5756-5767.
33. Poussier S, Thoquet P, Trigalet-Demery D, Barthet S, Meyer D, Arlat M et al. (2003). Host plant-dependent phenotypic reversion of Ralstonia solanacearum from non-pathogenic to pathogenic forms via alterations in the phcA gene. Mol Microbiol 49: 991-1003.
34. Ramette A, LiPuma JJ, Tiedje JM. (2005). Species abundance and diversity of Burkholderia cepacia complex in the environment. Appl Environ Microbiol 71: 1193-1201.
35. Reik R, Spilker T, Lipuma JJ. (2005). Distribution of Burkholderia cepacia complex species among isolates recovered from persons with or without cystic fibrosis. J Clin Microbiol 43: 2926-2928.
36. Rosenfeld Y, Shai Y. (2006). Lipopolysaccharide (Endotoxin)-host defense antibacterial peptides interactions: role in bacterial resistance and prevention of sepsis. Biochim Biophys Acta 1758: 1513-1522.
37. Saini LS, Galsworthy SB, John MA, Valvano MA. (1999). Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145(Pt 12): 3465-3475.
38. Sajjan SU, Carmody LA, Gonzalez CF, LiPuma JJ. (2008). A type IV secretion system contributes to intracellular survival and replication of Burkholderia cenocepacia. Infect Immun 76: 5447-5455.
39. Sajjan US, Yang JH, Hershenson MB, LiPuma JJ. (2006). Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells. Cell Microbiol 8: 1456-1466.
40. Savoia D, Zucca M. (2007). Clinical and environmental Burkholderia strains: biofilm production and intracellular survival. Curr Microbiol 54: 440-444.
41. Seed KD, Dennis JJ. (2008). Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 76: 1267-1275.
42. Segura I, Casadesus J, Ramos-Morales F. (2004). Use of mixed infections to study cell invasion and intracellular proliferation of Salmonella enterica in eukaryotic cell cultures. J Microbiol Methods 56: 83-91.
43. Valvano MA, Keith KE, Cardona ST. (2005). Survival and persistence of opportunistic Burkholderia species in host cells. Curr Opin Microbiol 8: 99-105.
44. van der Woude MW, Baumler AJ. (2004). Phase and antigenic variation in bacteria. Clin Microbiol Rev 17: 581-611.
45. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ et al. (2009). Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59: 102-111.
46. Vial L, Lépine F, Milot S, Groleau MC, Dekimpe V, Woods DE et al. (2008). Burkholderia pseudomallei, B. thailandensis, and B. ambifaria produce 4-hydroxy-2-alkylquinoline analogues with a methyl group at the 3 position that is required for quorum-sensing regulation. J Bacteriol 190: 5339-5352.
47. Villemur R, Déziel E. (2005). Phase variation and antigenic variation. In: Mullany P (ed) The Dynamic Bacterial Genome. Cambridge University Press: New York. pp 277-322.
48. Wisniewski-Dyé F, Vial L. (2008). Phase and antigenic variation mediated by genome modifications. Antonie Van Leeuwenhoek 94: 493-515.
49. Wopperer J, Cardona ST, Huber B, Jacobi CA, Valvano MA, Eberl L. (2006). A quorum-quenching approach to investigate the conservation of quorum-sensing-regulated functions within the Burkholderia cepacia complex. Appl Environ Microbiol 72: 1579-1587.
50. Zhou H, Yao F, Roberts DP, Lessie TG. (2003). AHLdeficient mutants of Burkholderia ambifaria BC-F have decreased antifungal activity. Curr Microbiol 47: 174-179.
51. Zlosnik JE, Hird TJ, Fraenkel MC, Moreira LM, Henry DA, Speert DP. (2008). Differential mucoid exopolysaccharide production by members of the Burkholderia cepacia complex. J Clin Microbiol 46: 1470-1473.