Advertisement

Applied Microbiology and Biotechnology

, Volume 87, Issue 1, pp 31–40 | Cite as

Pathogenicity, virulence factors, and strategies to fight against Burkholderia cepacia complex pathogens and related species

  • Jorge H. Leitão
  • Sílvia A. Sousa
  • Ana S. Ferreira
  • Christian G. Ramos
  • Inês N. Silva
  • Leonilde M. Moreira
Mini-Review

Abstract

The Burkholderia cepacia complex (Bcc) is a group of 17 closely related species of the β-proteobacteria subdivision that emerged in the 1980s as important human pathogens, especially to patients suffering from cystic fibrosis. Since then, a remarkable progress has been achieved on the taxonomy and molecular identification of these bacteria. Although some progress have been achieved on the knowledge of the pathogenesis traits and virulence factors used by these bacteria, further work envisaging the identification of potential targets for the scientifically based design of new therapeutic strategies is urgently needed, due to the very difficult eradication of these bacteria with available therapies. An overview of these aspects of Bcc pathogenesis and opportunities for the design of future therapies is presented and discussed in this work.

Keywords

Burkholderia cepacia complex Pathogenicity Virulence factors Antimicrobials 

Notes

Acknowledgments

This work was funded by FEDER and Fundação para a Ciência e Tecnologia (FCT), Portugal, through contracts PTDC/BIA-MIC/66977/2006 and PTDC/EBB-BIO/098352/2008, a post-doctoral grant to SAS and PhD grants to ASF and INS. A doctoral grant from Fundação Calouste Gulbenkian (FCG) to CGR is also acknowledged.

References

  1. Agnoli K, Lowe CA, Farmer KL, Husnain SI, Thomas MS (2006) The ornibactin biosynthesis and transport genes of Burkholderia cenocepacia are regulated by an extracytoplasmic function s factor which is a part of the Fur regulon. J Bacteriol 188:3631–3644Google Scholar
  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 cepacia. Infect Immun 76:1979–1991CrossRefGoogle Scholar
  3. Ball R, Brownlee KG, Duff AJ, Denton M, Conway SP, Lee TW (2010) Can Burkholderia cepacia complex be eradicated with nebulised Amiloride and TOBI? J Cyst Fibros 9(1):51–55CrossRefGoogle Scholar
  4. Bernier SP, Sokol PA (2005) Use of suppression-subtractive hybridization to identify genes in the Burkholderia cepacia complex that are unique to Burkholderia cenocepacia. J Bacteriol 187:5278–5291CrossRefGoogle Scholar
  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 71:5306–5313CrossRefGoogle Scholar
  6. Bernier SP, Nguyen DT, Sokol PA (2008) A LysR-type transcriptional regulator in Burkholderia cenocepacia influences colony morphology and virulence. Infect Immun 76:38–47CrossRefGoogle Scholar
  7. Boucher RC (2007) Evidence for airway surface dehydration as the initiating event in CF airway disease. J Intern Med 261:5–16CrossRefGoogle Scholar
  8. Burkholder W (1950) Sour skin, a bacterial rot of onion bulbs. Phytopathol 64:468–475Google Scholar
  9. Burns JL, Jonas M, Chi EY, Clark DK, Berger A, Griffith A (1996) Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 64:4054–4059Google Scholar
  10. Bylund J, Burgess LA, Cescutti P, Ernst RK, Speert D (2006) Exopolysaccharides from Burkholderia cenocepacia inhibit neutrophil chemotaxis and scavenge reactive oxygen species. J Biol Chem 281:2526–2532CrossRefGoogle Scholar
  11. Caraher E, Reynolds G, Murphy P, McClean S, Callaghan M (2007) Comparison of antibiotic susceptibility of Burkholderia cepacia complex organisms when grown planktonically or as biofilm in vitro. Eur J Clin Microbiol Infect Dis 26:213–216CrossRefGoogle Scholar
  12. 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 250:97–104CrossRefGoogle Scholar
  13. Cescutti P, Bosco M, Picotti F, Impallomeni G, Leitão JH, Richau JA, Sá-Correia I (2000) Structural study of the exopolysaccharide produced by a clinical isolate of Burkholderia cepacia. Biochem Biophys Res Commun 273:1088–1094CrossRefGoogle Scholar
  14. Cheung KJ Jr, Li G, Urban TA, Goldberg JB, Griffith A, Lu F, Burns JL (2007) Pilus-mediated epithelial cell death in response to infection with Burkholderia cenocepacia. Microbes Infect 9:829–837CrossRefGoogle Scholar
  15. Chu KK, Davidson DJ, Halsey TK, Chung JW, Speert DP (2002) Differential persistence among genomovars of the Burkholderia cepacia complex in a murine model of pulmonary infection. Infect Immun 70:2715–2720CrossRefGoogle Scholar
  16. Chung JW, Altman E, Beveridge TJ, Speert DP (2003) Colonial morphology of Burkholderia cepacia complex genomovar III: implications in exopolysaccharide production, pilus expression, and persistence in the mouse. Infect Immun 71:904–909CrossRefGoogle Scholar
  17. Cieri M, Mayer-Hamblett N, Griffith A, Burns JL (2002) Correlation between an in vitro invasion assay and a murine model of Burkholderia cepacia lung infection. Infect Immun 70:1081–1086CrossRefGoogle Scholar
  18. Coenye T, Vandamme P, Govan JRW, LiPuma JJ (2001) Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39:3427–3436CrossRefGoogle Scholar
  19. Conway BA, Chu KK, Bylund J, Altman E, Speert DP (2004) Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell-surface interactions and altered bacterial clearance in mice. J Infect Dis 190:957–966CrossRefGoogle Scholar
  20. Corbett CR, Burtnick MN, Kooi C, Woods DE, Sokol PA (2003) An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149:2263–2271CrossRefGoogle Scholar
  21. Cunha MV, Sousa SA, Leitão JH, Moreira LM, Videira PA, 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 42:3052–3058CrossRefGoogle Scholar
  22. Cunha MV, Pinto-de-Oliveira A, Meirinhos-Soares L, Salgado MJ, Melo-Cristino J, Correia S, Barreto C, Sá-Correia I (2007) Exceptionally high representation of Burkholderia cepacia among the B. cepacia complex isolates recovered from the major portuguese Cystic Fibrosis center. J Clin Microbiol 45:1582–1588CrossRefGoogle Scholar
  23. Davidson DJ, Dorin JR, McLachlan G, Ranaldi V, Lamb D, Doherty C, Govan J, Porteous DJ (1995) Lung disease in the cystic fibrosis mouse exposed to bacterial pathogens. Nat Genet 9:351–357CrossRefGoogle Scholar
  24. Deng Y, Boon C, Eberl L, Zhang LH (2009) Differential modulation of Burkholderia cenocepacia virulence and energy metabolism by the quorum-sensing signal BDSF and its synthase. J Bacteriol 191:7270–7278CrossRefGoogle Scholar
  25. Diggle SP, Lumjiaktase P, Dipilato F, Winzer K, Kunakorn M, Barrett D, Chhabra SR, Camara M, Williams P (2006) Functional genetic analysis reveals a 2-alkyl-4-quinolone signaling system in the human pathogen Burkholderia pseudomallei and related bacteria. Chemistry & Biology 13:701–710Google Scholar
  26. Engledow AS, Medrano EG, Mahenthiralingam E, LiPuma JJ, Gonzalez CF (2004) Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia. J Bacteriol 186:6015–6024CrossRefGoogle Scholar
  27. Fauré R, Shiao T, Lagnoux D, Giguère D, Roy R (2007) En route to a carbohydrate-based vaccine against Burkholderia cepacia. Org Biomol Chem 5:2704–2708Google Scholar
  28. Fehlner-Gardiner CC, Hopkins TM, Valvano MA (2002) Identification of a general secretory pathway in a human isolate of Burkholderia vietnamiensis (formerly B. cepacia complex genomovar V) that is required for the secretion of hemolysin and phospholipase C activities. Microb Pathog 32:249–254CrossRefGoogle Scholar
  29. Ferreira AS, Leitão JH, Sousa SA, Cosme AM, Sá-Correia I, Moreira LM (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 73:524–534CrossRefGoogle Scholar
  30. Ferreira AS, Leitão JH, Silva IN, Pinheiro PF, Sousa SA, Ramos CG, Moreira LM (2010) Distribution of cepacian biosynthetic genes among environmental and clinical strains of the Burkholderia genus and role of this exopolysaccharide on resistance to stress conditions. Appl Environ Microbiol 76:441–450CrossRefGoogle Scholar
  31. Gibson RL, Burns JL, Ramsey BW (2003) Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168:918–951CrossRefGoogle Scholar
  32. Gingues S, Kooi C, Visser MB, Subsin B, Sokol PA (2005) Distribution and expression of the ZmpA metalloprotease in the Burkholderia cepacia complex. J Bacteriol 187:8247–8255CrossRefGoogle Scholar
  33. Gonzalez CF, Vidaver AK (1979) Bacteriocin, plasmid and pectolytic diversity in Pseudomonas cepacia of clinical and plant origin. J Gen Microbiol 110:161–170Google Scholar
  34. Gonzalez CF, Pettit EA, Valadez VA, Provin EM (1997) Mobilization, cloning, and sequence determination of a plasmid-encoded polygalacturonase from a phytopathogenic Burkholderia (Pseudomonas) cepacia. Mol Plant Microbe Interact 10:840–851CrossRefGoogle Scholar
  35. Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574Google Scholar
  36. Govan JR, Brown PH, Maddison J, Doherty CJ, Nelson JW, Dodd M, Greening AP, Webb AK (1993) Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 342:15–19CrossRefGoogle Scholar
  37. Govan JR, Brown AR, Jones AM (2007) Evolving epidemiology of Pseudomonas aeruginosa and Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol 2:153–164CrossRefGoogle Scholar
  38. Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, Cerdeno-Tarraga AM, Thomson NR, Bason N, Quail MA, Sharp S, Cherevach I, Churcher C, Goodhead I, Hauser H, Holroyd N, Mungall K, Scott P, Walker D, White B, Rose H, Iversen P, Mil-Homens D, Rocha EP, Fialho AM, Baldwin A, Dowson C, Barrell BG, Govan JR, Vandamme P, Hart CA, Mahenthiralingam E, Parkhill J (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191:261–277CrossRefGoogle Scholar
  39. Hunt TA, Kooi C, Sokol PA, Valvano MA (2004) Identification of Burkholderia cenocepacia genes required for bacterial survival in vivo. Infect Immun 72:4010–4022CrossRefGoogle Scholar
  40. Hutchison ML, Poxton IR, Govan JR (1998) Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect Immun 66:2033–2039Google Scholar
  41. Hutchison ML, Bonell EC, Poxton IR, Govan JR (2000) Endotoxic activity of lipopolysaccharides isolated from emergent potential cystic fibrosis pathogens. FEMS Immunol Med Microbiol 27:73–77CrossRefGoogle Scholar
  42. Isles A, Macluski I, Corey M, Gold R, Prober C, Fleming P, Levison H (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104:206–210CrossRefGoogle Scholar
  43. Jacquot J, Tabary O, Le Rouzic P, Clement A (2008) Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol 40:1703–1715CrossRefGoogle Scholar
  44. Keig PM, Ingham E, Kerr KG (2001) Invasion of human type II pneumocytes by Burkholderia cepacia. Microb Pathog 30:167–170CrossRefGoogle Scholar
  45. Kooi C, Subsin B, Chen R, Pohorelic B, Sokol P (2006) Burkholderia cenocepacia ZmpB is a broadly-specificity zinc metallo-protease involved in virulence. Infect Immun 74:4083–4093CrossRefGoogle Scholar
  46. Köthe M, Antl M, Huber B, Stoecker K, Ebrecht D, Steinmetz I, Eberl L (2003) Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell Microbiol 5:343–51CrossRefGoogle Scholar
  47. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore mediated signalling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 99:7072–7077Google Scholar
  48. Lamothe J, Thyssen S, Valvano MA (2004) Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell Microbiol 6:1127–138CrossRefGoogle Scholar
  49. Laws TR, Smith SA, Smith MP, Harding SV, Atkins TP, Titball RW (2005) The nematode Panagrellus redivivus is susceptible to killing by human pathogens at 37 degrees C. FEMS Microbiol Lett 250:77–83CrossRefGoogle Scholar
  50. Leitão JH, Sousa SA, Cunha MV, Salgado MJ, Melo-Cristino J, Barreto MC, Sá-Correia I (2008) Variation of the antimicrobial susceptibility profiles of Burkholderia cepacia complex clonal isolates obtained from chronically infected cystic fibrosis patients: a five-year survey in the major Portuguese treatment center. Eur J Clin Microbiol Infect Dis 27:1101–1111CrossRefGoogle Scholar
  51. Lewenza S, Sokol PA (2001) Regulation of ornibactin biosynthesis and N-acyl-Lhomoserine lactone production by CepR in Burkholderia cepacia. J Bacteriol 183:2212–2218Google Scholar
  52. Loutet SA, Bartholdson SJ, Govan JR, Campopiano DJ, Valvano MA (2009) Contributions of two UDP-glucose dehydrogenases to viability and polymyxin B resistance of Burkholderia cenocepacia. Microbiology 155:2029–2039CrossRefGoogle Scholar
  53. Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539–1551CrossRefGoogle Scholar
  54. Makidon PE, Knowlton J, Groom JV 2nd, Blanco LP, Lipuma JJ, Bielinska AU, Baker JR Jr (2010) Induction of immune response to the 17 kDa OMPA Burkholderia cenocepacia polypeptide and protection against pulmonary infection in mice after nasal vaccination with an OMP nanoemulsion-based vaccine. Med Microbiol Immunol. doi: 10.1007/s00430-009-0137-2 Google Scholar
  55. Malott RJ, Sokol PA (2007) Expression of the bviIR and cepIR quorum-sensing systems of Burkholderia vietnamiensis. J Bacteriol 189:3006–3016CrossRefGoogle Scholar
  56. Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73:4982–4992CrossRefGoogle Scholar
  57. Marier JF, Lavigne J, Ducharme MP (2002) Pharmacokinetics and efficacies of liposomal and conventional formulations of tobramycin after intratracheal administration in rats with pulmonary Burkholderia cepacia infection. Antimicrob Agents Chemother 46:3776–3781CrossRefGoogle Scholar
  58. Marolda CL, Hauröder 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 145:1509–1517CrossRefGoogle Scholar
  59. McClean S, Callaghan M (2009) Burkholderia cepacia complex: epithelial cell-pathogen confrontations and potential for therapeutic intervention. J Med Microbiol 58:1–12CrossRefGoogle Scholar
  60. Mil-Homens D, Rocha EPC, Fialho AM (2010) Genome-wide analysis of DNA repeats in Burkholderia cenocepacia J2315 identifies a novel adhesin-like gene unique to epidemic-associated strains of the ET-12 lineage. Microbiology 156:1084–1096Google Scholar
  61. Moreira LM, Videira PA, Sousa SA, Leitão JH, Cunha MV, 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 312:323–3133CrossRefGoogle Scholar
  62. Mullen T, Markey K, Murphy P, McClean S, Callaghan M (2007) Role of lipase in Burkholderia cepacia complex (Bcc) invasion of lung epithelial cells. Eur J Clin Microbiol Infect Dis 26:869–877CrossRefGoogle Scholar
  63. O’Malley CA (2009) Infection control in cystic fibrosis: cohorting, cross-contamination, and the respiratory therapist. Respir Care 54:641–657CrossRefGoogle Scholar
  64. 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 9:1017–1134CrossRefGoogle Scholar
  65. Pirone L, Bragonzi A, Farcomeni A, Paroni M, Auriche C, Conese M, Chiarini L, Dalmastri C, Bevivino A, Ascenzioni F (2008) Burkholderia cenocepacia strains isolated from cystic fibrosis patients are apparently more invasive and more virulent than rhizosphere strains. Environ Microbiol 10:2773–2784Google Scholar
  66. Richau JA, Leitão JH, Correia M, Lito L, Salgado MJ, Barreto C, Cescutti P, Sá-Correia I (2000) Molecular typing and exopolysaccharide biosynthesis of Burkholderia cepacia isolates from a Portuguese cystic fibrosis center. J Clin Microbiol 38:1651–1655Google Scholar
  67. Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H, Høiby N, Givskov M, Molin S, Eberl L (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:3249–3262Google Scholar
  68. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok J, Plasic S, Chou J-L, Drumm ML, Ianuzzi MC, Collins FS, Tsui L-C (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066–1073CrossRefGoogle Scholar
  69. Saini LS, Galsworthy SB, John MA, Valvano MA (1999) Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145:3465–3475Google Scholar
  70. Sajjan U, Thanassoulis G, Cherapanov V, Lu A, Sjolin C, Steer B, Wu YJ, Rotstein OD, Kent G, McKerlie C, Forstner J, Downey GP (2001) Enhanced susceptibility to pulmonary infection with Burkholderia cepacia in Cftr(-/-) mice. Infect Immun 69:5138–5150CrossRefGoogle Scholar
  71. Sajjan U, Keshavjee S, Forstner J (2004) Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection. Infect Immun 72:4188–4199CrossRefGoogle Scholar
  72. 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 8:1456–1466CrossRefGoogle Scholar
  73. Sajjan US, Carmody LA, Gonzalez CF, LiPuma JJ (2008) A type IV secretion system contributes to intracellular survival and replication of Burkholderia cenocepacia. Infect Immun 76:5447–5455CrossRefGoogle Scholar
  74. Saldías MS, Valvano MA (2009) Interactions of Burkholderia cenocepacia and other Burkholderia cepacia complex bacteria with epithelial and phagocytic cells. Microbiology 155:2809–2817CrossRefGoogle Scholar
  75. Saldias MS, Lamothe J, Wu R, Valvano MA (2008) Burkholderia cenocepacia requires the RpoN sigma factor for biofilm formation and intracellular trafficking within macrophages. Infect Immun 76:1059–1067Google Scholar
  76. Seed KD, Dennis JJ (2008) Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 76:1267–1275CrossRefGoogle Scholar
  77. Seed KD, Dennis JJ (2009) Experimental bacteriophage therapy increases survival of Galleria mellonella larvae infected with clinically relevant strains of the Burkholderia cepacia complex. Antimicrob Agents Chemother 53:2205–2208CrossRefGoogle Scholar
  78. Schulein R, Dehio C (2002) The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol Microbiol 46:1053–1076Google Scholar
  79. Schwab U, Leigh M, Ribeiro C, Yankaskas J, Burns K, Gilligan P, Sokol P, Boucher R (2002) Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect Immun 70:4547–4555CrossRefGoogle Scholar
  80. Sokol PA, Sajjan U, Visser MB, Gingues S, Forstner J, Kooi C (2003) The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149:3649–3658CrossRefGoogle Scholar
  81. Sokol PA, Malott RJ, Riedel K, Eberl (2007) Communication systems in the genus Burkholderia: global regulators and targets for novel antipathogenic drugs. Future Microbiol 2:555–563CrossRefGoogle Scholar
  82. Sousa SA, Ulrich M, Bragonzi A, Burke M, Worlitzsch D, Leitão JH, Meisner C, Eberl L, Sá-Correia I, Döring G (2007a) Virulence of Burkholderia cepacia complex strains in gp91phox-/-mice. Cell Microbiol 9:2817–2825CrossRefGoogle Scholar
  83. Sousa SA, Moreira LM, Wopperer J, Eberl L, Sá-Correia I, Leitão JH (2007b) The Burkholderia cepacia bceA gene encodes a protein with phosphomannose isomerase and GDP-D-mannose pyrophosphorylase activities. Biochem Biophys Res Commun 353:200–206CrossRefGoogle Scholar
  84. Sousa SA, Moreira LM, Leitão JH (2008a) Functional analysis of the Burkholderia cenocepacia J2315 BceAJ protein with phosphomannose isomerase and GDP-D-mannose pyrophosphorylase activities. Appl Microbiol Biotechnol 80:1015–1022CrossRefGoogle Scholar
  85. Sousa SA, Ramos CG, Almeida F, Meirinhos-Soares L, Wopperer J, Schwager S, Eberl L, Leitão JH (2008b) Burkholderia cenocepacia J2315 acyl carrier protein: a potential target for antimicrobials’ development? Microb Pathog 45:331–336CrossRefGoogle Scholar
  86. Sousa SA, Ramos CG, Moreira LM, Leitão JH (2010) The hfq gene is required for stress resistance and full virulence of Burkholderia cepacia to the nematode Caenorhabditis elegans. Microbiology 156:896–908CrossRefGoogle Scholar
  87. Starke JR, Edwards MS, Langston C, Baker CJ (1987) A mouse model of chronic pulmonary infection with Pseudomonas aeruginosa and Pseudomonas cepacia. Pediatr Res 22:698–702CrossRefGoogle Scholar
  88. Tilley LD, Mellbye BL, Puckett SE, Iversen PL, Geller BL (2007) Antisense peptide-phosphorodiamidate morpholino oligomer conjugate: dose-response in mice infected with Escherichia coli. J Antimicrob Chemother 59:66–73Google Scholar
  89. Tomich M, Griffith A, Herfst CA, Burns JL, Mohr CD (2003) Attenuated virulence of a Burkholderia cepacia type III secretion mutant in a murine model of infection. Infect Immun 71:1405–1415CrossRefGoogle Scholar
  90. Uehlinger S, Schwager S, Bernier SP, Riedel K, Nguyen DT, Sokol PA, Eberl L (2009) Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect Immun 77:4102–4110CrossRefGoogle Scholar
  91. Urban TA, Griffith A, Torok AM, Smolkin ME, Burns JL, Goldberg JB (2004) Contribution of Burkholderia cenocepacia flagella to infectivity and inflammation. Infect Immun 72:5126–5134CrossRefGoogle Scholar
  92. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (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 59:102–111CrossRefGoogle Scholar
  93. Vanlaere E, Lipuma JJ, Baldwin A, Henry D, De Brandt E, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2008) Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 58:1580–1590CrossRefGoogle Scholar
  94. Venturi V, Friscina A, Bertani I, Devescovi G, Aguilar C (2004) Quorum sensing in the Burkholderia cepacia complex. Res Microbiol 155:238–244CrossRefGoogle Scholar
  95. Videira PA, Garcia AP, Sá-Correia I (2005) Functional and topological analysis of the Burkholderia cenocepacia priming glucosyltransferase BceB, involved in the biosynthesis of the cepacian exopolysaccharide. J Bacteriol 187:5013–5018CrossRefGoogle Scholar
  96. Vinion-Dubiel AD, Goldberg JB (2003) Lipopolysaccharide of Burkholderia cepacia complex. J Endotoxin Res 9:201–213Google Scholar
  97. Wigley P, Burton NF (1999) Genotypic and phenotypic relationships in Burkholderia cepacia isolated from cystic fibrosis patients and the environment. J Appl Microbiol 86:460–468CrossRefGoogle Scholar
  98. Whitby PW, VanWagoner TM, Taylor AA, Seale TW, Morton DJ, LiPuma JJ, Stull TL (2006) Identification of an RTX determinant of Burkholderia cenocepacia J2315 by subtractive hybridization. J Med Microbiol 55:11–21CrossRefGoogle Scholar
  99. Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M (1992) Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Pseudomonas cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 36:1251–1275Google Scholar
  100. Yohalem DS, Lorbeer JW (1994) Intraspecific metabolic diversity among strains of Burkholderia cepacia isolated from decayed onions, soils, and the clinical environment. Antonie Van Leeuwenhoek 65:111–131CrossRefGoogle Scholar
  101. Zhang R, LiPuma JJ, Gonzalez CF (2009) Two type IV secretion systems with different functions in Burkholderia cenocepacia K56-2. Microbiology 155:4005–4013CrossRefGoogle Scholar
  102. 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 46:1470–1473CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jorge H. Leitão
    • 1
  • Sílvia A. Sousa
    • 1
  • Ana S. Ferreira
    • 1
  • Christian G. Ramos
    • 1
  • Inês N. Silva
    • 1
  • Leonilde M. Moreira
    • 1
  1. 1.IBB—Institute for Biotechnology and Bioengineering, Centre for Biological and Chemical Engineering, Instituto Superior TécnicoLisbonPortugal

Personalised recommendations