Skip to main content

Advertisement

SpringerLink
Log in

Clinical and Environmental Burkholderia Strains: Biofilm Production and Intracellular Survival

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Bacteria belonging to the Burkholderia species are important pulmonary pathogens in cystic fibrosis (CF) patients. Their ability to establish chronic and sometimes fatal infections seems linked to the quorum sensing-regulated expression of virulence factors. We examined 23 Burkholderia isolates, 19 obtained from CF patients and 4 from the environment, to evaluate their ability to form biofilm and to penetrate and replicate inside J774 macrophagic cells. Our results indicate that biofilm formation and intracellular survival are behavioral traits frequently expressed by Burkholderia strains isolated from CF patients. Successive isolates obtained from each of four chronically infected patients yielded bacteria consistently belonging to the same strain but showing increasing ability to replicate intracellularly and to produce biofilm, possibly due to in vivo bacterial microevolution driven by the selective lung environmental conditions. Protection against antimicrobials granted to burkholderiae by the expression of these two virulence factors might account for the frequent failures of antibiotic treatment in CF patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature Cited

  1. Allice T, Scutera S, Chirillo MG, Savoia D (2006) Burkholderia respiratory tract infections in Italian patients with cystic fibrosis: molecular characterization. J Infect 53:159–165

    Article  PubMed  CAS  Google Scholar 

  2. Balandreau J, Viallard V, Cournoyer B, Coenye T, Laevens S, Vandamme P (2001) Burkholderia cepacia genomovar III is a common plant associated bacterium. Appl Environ Microbiol 67:982–985

    Article  PubMed  CAS  Google Scholar 

  3. Burns JL, Jonas M, Chi EY, Clark DK, Berger A, Griffith A (1996) Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 64:4054–4059

    PubMed  CAS  Google Scholar 

  4. Campana S, Taccetti G, Rivenni N, Favari F, Cariani L, Sciacca A, Savoia D, Collura A, Fiscarelli E, De Intinis G, Busetti M, Cipollini A, d’Aprile A, Provengano E, Collebrusco I, Frontini P, Stassi G, Trancassini M, Tovagliati D, Lavitola A, Doherty CJ, Coenye T, Govan JRW, Vandamme P (2005) Transmission of Burkholderia cepacia complex: evidence for new epidemic clones infecting cystic fibrosis patients in Italy. J Clin Microbiol 43:5136–5142

    Article  PubMed  CAS  Google Scholar 

  5. 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

    Article  PubMed  CAS  Google Scholar 

  6. Clode FE, Kaufmann ME, Malnick H, Pitt TL (1999) Evaluation of three oligonucleotide primer sets in PCR for identification of Burkholderia cepacia and their differentiation from Burkholderia gladioli. J Clin Pathol 52:173–176

    PubMed  CAS  Google Scholar 

  7. Coenye T, Vandamme P, Govan JRW, LiPuma JJ (2001) Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39:3427–3436

    Article  PubMed  CAS  Google Scholar 

  8. Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729

    Article  PubMed  CAS  Google Scholar 

  9. Cunha MV, Sousa SA, Leitao JH, Moreira LM, Videira PA, Sà-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

    Article  PubMed  CAS  Google Scholar 

  10. Djordjevic D, Wiedmann M, McLandsborough LA (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950–2958

    Article  PubMed  CAS  Google Scholar 

  11. Goss CH, Rosenfeld M (2004) Update on cystic fibrosis epidemiology. Curr Opin Pulm Med 10:510–514

    Article  PubMed  Google Scholar 

  12. 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 342:15–19

    Article  PubMed  CAS  Google Scholar 

  13. Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574

    PubMed  CAS  Google Scholar 

  14. Holmes A, Govan JRW, Goldstein R (1998) Agricultural use of Burkholderia (Pseudomonas) cepacia: a threat to human health? Emerg Infect Dis 4:221–227

    Article  PubMed  CAS  Google Scholar 

  15. Holmes A, Nolan R, Taylor R, Finley R, Riley M, Jiang R, Steinbach S, Goldstein R (1999) An epidemic of Burkholderia cepacia transmitted between patients with and without cystic fibrosis. J Infect Dis 179:1197–1205

    Article  PubMed  CAS  Google Scholar 

  16. Keig PM, Ingham E, Kerr KG (2001) Invasion of human type II pneumocytes by Burkholderia cepacia. Microb Pathog 30:167–170

    Article  PubMed  CAS  Google Scholar 

  17. Keig PM, Ingham E, Vandamme P, Kerr KG (2002) Differential invasion of respiratory epithelial cells by members of the Burkholderia cepacia complex. Clin Microbiol Infect 8:47–49

    Article  PubMed  CAS  Google Scholar 

  18. Khmel IA (2006) Quorum-sensing regulation of gene expression: fundamental and applied aspects and the role in bacterial communication. Microbiology 75:390–397

    Article  CAS  Google Scholar 

  19. Lamothe J, Huynh K, Grinstein S, Valvano MA (2006) Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell Microbiol 9:40–53

    Article  CAS  Google Scholar 

  20. LiPuma JJ, Dasen SE, Nielson DW, Stern RC, Stull TL (1990) Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet 336:1094–1096

    Article  PubMed  CAS  Google Scholar 

  21. LiPuma JJ (2005) Update on the Burkholderia cepacia complex. Curr Opin Pulm Med 11:528–533

    Article  PubMed  Google Scholar 

  22. Mahenthiralingam E, Simpson D, Speert DP (1997) Identification and characterization of a novel DNA marker associated with epidemic Burkholderia cepacia strains recovered from patients with cystic fibrosis. J Clin Microbiol 35:808–816

    PubMed  CAS  Google Scholar 

  23. Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156

    Article  PubMed  CAS  Google Scholar 

  24. Maloney KE, Valvano MA (2006) The mgtC gene of Burkholderia cenocepacia is required for growth under magnesium limitation conditions and intracellular survival in macrophages. Infect Immun 74:5477–5486

    Article  PubMed  CAS  Google Scholar 

  25. Martin DW, Mohr CD (2000) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68:24–29

    Article  PubMed  CAS  Google Scholar 

  26. Moxon R, Bayliss C, Hood D (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40:307–333

    Article  PubMed  CAS  Google Scholar 

  27. Nelson JW, Butler SL, Krieg D, Govan JRW (1994) Virulence factors of Burkholderia cepacia. FEMS Immunol Med Microbiol 8:89–98

    Article  PubMed  CAS  Google Scholar 

  28. Prouzet-Mauleon V, Hussain MA, Lamouliatte H, Kauser F, Megraud F, Ahmed N (2005) Pathogen evolution in vivo: genome dynamics of two isolates obtained 9 years apart from a duodenal ulcer patient infected with a single Helicobacter pylori strain. J Clin Microbiol 43:4237–4241

    Article  PubMed  CAS  Google Scholar 

  29. Saini LS, Galsworthy SB, John MA, Valvano MA (1999) Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145:3465–3475

    PubMed  CAS  Google Scholar 

  30. Sajjan US, Sylvester FA, Forstner J (2000) Cable-piliated Burkholderia cepacia bind to citokeratin 13 of epithelial cells. Infect Immun 68:1787–1795

    Article  PubMed  CAS  Google Scholar 

  31. 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: 4547–4555

    Article  PubMed  CAS  Google Scholar 

  32. Sun L, Jiang RZ, Steinbach S, Holmes A, Campanelli C, Forstner J, Sajjan U, Riley M, Goldstein R (1995) The emergence of a highly transmissible lineage of cbl+Pseudomonas (Burkholderia) cepacia causing CF centre epidemics in North America and Britain. Nat Med 1:661–666

    Article  PubMed  CAS  Google Scholar 

  33. Yassien M, Khardori N, Ahmedy A, Toama T (1995) Modulation of biofilm of P. aeruginosa by quinolones. Antimicrob Agents Chemother 39:2262–2268

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was partly supported by grants from the Italian Ministry for University and Scientific Research (ex 60%) and from Regione Piemonte (2004).

Author information

Authors and Affiliations

  1. Department of Clinical and Biological Sciences, University of Torino, S. Luigi Gonzaga Hospital, 10043, Orbassano, Torino, Italy

    Dianella Savoia & Mario Zucca

Authors
  1. Dianella Savoia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mario Zucca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dianella Savoia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Savoia, D., Zucca, M. Clinical and Environmental Burkholderia Strains: Biofilm Production and Intracellular Survival. Curr Microbiol 54, 440–444 (2007). https://doi.org/10.1007/s00284-006-0601-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-006-0601-9

Keywords

Search

Navigation