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Published in: Antimicrobial Resistance & Infection Control 1/2017

Open Access 01-12-2017 | Research

Virulence traits associated with Burkholderia cenocepacia ST856 epidemic strain isolated from cystic fibrosis patients

Authors: Milka Malešević, Zorica Vasiljević, Aleksandar Sovtić, Brankica Filipić, Katarina Novović, Milan Kojić, Branko Jovčić

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2017

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Abstract

Background

Burkholderia cenocepacia is considered one of the most problematic cystic fibrosis (CF) pathogens. Colonization prevalence in the Serbian CF population is high and virtually exclusively limited to a single highly transmissible clone of B. cenocepacia ST856 which is positive for both the B. cepacia epidemic strain marker (BCESM) and cable pilin, and is closely related to the epidemic strain CZ1 (ST32).

Methods

Biofilm formation for 182 isolates, and adhesion to components of the host extracellular matrix, proteolytic activity, mucoidy and motility of selected ST856 representatives, as well as B. cenocepacia ST858 and ST859, and B. stabilis ST857, novel STs isolated from Serbian CF patients, were investigated in this study. The presence of the cepI, cepR, fliG, llpE, wbiI, and bcscV genes was analyzed.

Results

Biofilm-formation ability of analyzed strains was poor under standard laboratory conditions, but changed in stress conditions (cold stress) and conditions that mimic CF milieu (increased CO2). All strains expressed ability to bind to collagen and fibronectin albeit with different intensity. Representatives of ST856 exhibited gelatinase activity. ST858, ST859 and 9/11 of ST856 genotypes were positive for swimming and twitching motility whereas ST857 was non-motile. Mucoidy was demonstrated in all ST856 genotypes, ST857 was semi-mucoid, and ST858 and ST859 were non-mucoid. Molecular analysis for major virulence factors revealed that ST856 and ST857 carried the six analyzed genes, while ST858 and ST859 were negative for the llpE gene.

Conclusion

Variations in virulence phenotypes in different genotypes of epidemic B. cenocepacia ST856 clone, in vitro, could be a consequence of diversification driven by pathoadaptation. Diversity of epidemic clone genotypes virulence, could be challenging for accurate diagnosis and treatment, as well as for infection control.
Literature
1.
go back to reference Folescu TW, da Costa CH, Cohen RWF, da Conceição Neto OC, Albano RM, Marques EA. Burkholderia cepacia complex: clinical course in cystic fibrosis patients. BMC Pul Med. 2015;15:158. doi:10.1186/s12890-015-0148-2.CrossRef Folescu TW, da Costa CH, Cohen RWF, da Conceição Neto OC, Albano RM, Marques EA. Burkholderia cepacia complex: clinical course in cystic fibrosis patients. BMC Pul Med. 2015;15:158. doi:10.​1186/​s12890-015-0148-2.CrossRef
2.
go back to reference Mahenthiralingam E, Baldwin A, Vandamme P. Burkholderia cepacia complex infection in patients with cystic fibrosis. J Med Microbiol. 2002;51:1–6.CrossRef Mahenthiralingam E, Baldwin A, Vandamme P. Burkholderia cepacia complex infection in patients with cystic fibrosis. J Med Microbiol. 2002;51:1–6.CrossRef
3.
go back to reference Drevinek P, Mahenthiralingam E. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect. 2010;16:821–30.CrossRefPubMed Drevinek P, Mahenthiralingam E. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect. 2010;16:821–30.CrossRefPubMed
4.
go back to reference Coenye T, Vandamme P. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol. 2003;5:719–29.CrossRefPubMed Coenye T, Vandamme P. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol. 2003;5:719–29.CrossRefPubMed
6.
go back to reference Tomich M, Griffith A, Herfst CA, Burns JL, Mohr CD. Attenuated virulence of a Burkholderia cepacia type III secretion mutant in a murine model of infection. Infect Immun. 2003;71:1405–15.CrossRefPubMedPubMedCentral Tomich M, Griffith A, Herfst CA, Burns JL, Mohr CD. Attenuated virulence of a Burkholderia cepacia type III secretion mutant in a murine model of infection. Infect Immun. 2003;71:1405–15.CrossRefPubMedPubMedCentral
7.
go back to reference Nair BN, Joachimiak LA, Chattopadhyay S, Montano I, Burns J. Conservation of a novel protein associated with an antibiotic efflux operon in Burkholderia cenocepacia. FEMS Microbiol Lett. 2005;245:337–44.CrossRefPubMed Nair BN, Joachimiak LA, Chattopadhyay S, Montano I, Burns J. Conservation of a novel protein associated with an antibiotic efflux operon in Burkholderia cenocepacia. FEMS Microbiol Lett. 2005;245:337–44.CrossRefPubMed
9.
go back to reference Ortega X, Hunt TA, Loutet S, Vinion-Dubiel AD, Datta A, Choudhury B, et al. Reconstitution of O-specific lipopolysaccharide expression in Burkholderia cenocepacia strain J2315, which is associated with transmissible infections in patients with cystic fibrosis. J Bacteriol. 2005;187:1324–33. Ortega X, Hunt TA, Loutet S, Vinion-Dubiel AD, Datta A, Choudhury B, et al. Reconstitution of O-specific lipopolysaccharide expression in Burkholderia cenocepacia strain J2315, which is associated with transmissible infections in patients with cystic fibrosis. J Bacteriol. 2005;187:1324–33.
10.
go back to reference Goldberg JB, Ganesan S, Comstock AT, Zhao Y, Sajjan US. Cable pili and the associated 22 kDa adhesin contribute to Burkholderia cenocepacia persistence in vivo. PLoS One. 2011;6(7):e22435.CrossRefPubMedPubMedCentral Goldberg JB, Ganesan S, Comstock AT, Zhao Y, Sajjan US. Cable pili and the associated 22 kDa adhesin contribute to Burkholderia cenocepacia persistence in vivo. PLoS One. 2011;6(7):e22435.CrossRefPubMedPubMedCentral
11.
go back to reference Speert DP, Henry D, Vandamme P, Corey M, Mahenthiralingam E. Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis. 2002;8:181–7.CrossRefPubMedPubMedCentral Speert DP, Henry D, Vandamme P, Corey M, Mahenthiralingam E. Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis. 2002;8:181–7.CrossRefPubMedPubMedCentral
12.
go back to reference Govan JR, Brown AR, Jones AM. Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol. 2007;2(2):153–64.CrossRefPubMed Govan JR, Brown AR, Jones AM. Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol. 2007;2(2):153–64.CrossRefPubMed
13.
go back to reference Vasiljevic Z, Novovic K, Kojic M, Sovtic A, Minic P, Djukic S, et al. Burkholderia cepacia complex in Serbian patients with cystic fibrosis: prevalence and molecular epidemiology. Eur J Clin Microbiol Infect Dis. 2016; doi:10.1007/s10096-016-2662-4. Vasiljevic Z, Novovic K, Kojic M, Sovtic A, Minic P, Djukic S, et al. Burkholderia cepacia complex in Serbian patients with cystic fibrosis: prevalence and molecular epidemiology. Eur J Clin Microbiol Infect Dis. 2016; doi:10.​1007/​s10096-016-2662-4.
14.
go back to reference Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40(2):175–9.CrossRefPubMed Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40(2):175–9.CrossRefPubMed
15.
16.
go back to reference Ahmed S, Meghji S, Williams RJ, Henderson B, Brock JH, Nair SP. Staphylococcus aureus fibronectin binding proteins are essential for internalization by osteoblasts but do not account for differences in intracellular levels of bacteria. Infect Immun. 2001;69:2872–7.CrossRefPubMedPubMedCentral Ahmed S, Meghji S, Williams RJ, Henderson B, Brock JH, Nair SP. Staphylococcus aureus fibronectin binding proteins are essential for internalization by osteoblasts but do not account for differences in intracellular levels of bacteria. Infect Immun. 2001;69:2872–7.CrossRefPubMedPubMedCentral
17.
go back to reference Lopes MF, Simões AP, Tenreiro R, Marques JJ, Crespo MT. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol. 2006;112(3):208–14.CrossRef Lopes MF, Simões AP, Tenreiro R, Marques JJ, Crespo MT. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol. 2006;112(3):208–14.CrossRef
19.
go back to reference Zlosnik J, Hird T, Fraenkel M, Moreira L, Henry D, Speert D. Differential mucoid exopolysaccharide production by members of the Burkholderia cepacia complex. J Clin Microbiol. 2008;46(4):1470–3.CrossRefPubMedPubMedCentral Zlosnik J, Hird T, Fraenkel M, Moreira L, Henry D, Speert D. Differential mucoid exopolysaccharide production by members of the Burkholderia cepacia complex. J Clin Microbiol. 2008;46(4):1470–3.CrossRefPubMedPubMedCentral
20.
go back to reference Trancassini M, Iebba V, Citerà N, Tuccio V, Magni A, Varesi P, et al. Outbreak of Achromobacter xylosoxidans in an Italian cystic fibrosis center: genome variability, biofilm production, antibiotic resistance, and motility in isolated strains. Front Microbiol. 2014;5:138. doi:10.3389/fmicb.2014.00138.CrossRefPubMedPubMedCentral Trancassini M, Iebba V, Citerà N, Tuccio V, Magni A, Varesi P, et al. Outbreak of Achromobacter xylosoxidans in an Italian cystic fibrosis center: genome variability, biofilm production, antibiotic resistance, and motility in isolated strains. Front Microbiol. 2014;5:138. doi:10.​3389/​fmicb.​2014.​00138.CrossRefPubMedPubMedCentral
21.
go back to reference Graindorge A, Menard A, Neto M, Bouvet C, Miollan R, Gaillard S, et al. 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. 2008;66:29–40.CrossRef Graindorge A, Menard A, Neto M, Bouvet C, Miollan R, Gaillard S, et al. 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. 2008;66:29–40.CrossRef
22.
go back to reference Sousa S, Ramos CG, Leitão JH. Burkholderia cepacia complex: emerging multihost pathogens equipped with a wide range of virulence factors and determinants. Int J Microbiol. 2011; doi:10.1155/2011/607575. Sousa S, Ramos CG, Leitão JH. Burkholderia cepacia complex: emerging multihost pathogens equipped with a wide range of virulence factors and determinants. Int J Microbiol. 2011; doi:10.​1155/​2011/​607575.
24.
go back to reference Schwab U, Abdullah LH, Perlmutt OS, Albert D, Davis CW, Arnold RR, et al. Localization of Burkholderia cepacia complex bacteria in cystic fibrosis lungs and interactions with Pseudomonas aeruginosa in hypoxic mucus. Infect Immun. 2014;82(11):4729–45. Schwab U, Abdullah LH, Perlmutt OS, Albert D, Davis CW, Arnold RR, et al. Localization of Burkholderia cepacia complex bacteria in cystic fibrosis lungs and interactions with Pseudomonas aeruginosa in hypoxic mucus. Infect Immun. 2014;82(11):4729–45.
25.
go back to reference Conway BD, Venu V, Speert DP. Biofilm formation and acyl homoserine lactone production in the Burkholderia cepacia complex. J Bacteriol. 2002;184(20):5678–85.CrossRefPubMedPubMedCentral Conway BD, Venu V, Speert DP. Biofilm formation and acyl homoserine lactone production in the Burkholderia cepacia complex. J Bacteriol. 2002;184(20):5678–85.CrossRefPubMedPubMedCentral
26.
go back to reference Tate S, MacGregor G, Davis M, Innes JA, Greening AP. Airways in cystic fibrosis are acidified: detection by exhaled breath condensate. Thorax. 2002;57:926–9.CrossRefPubMedPubMedCentral Tate S, MacGregor G, Davis M, Innes JA, Greening AP. Airways in cystic fibrosis are acidified: detection by exhaled breath condensate. Thorax. 2002;57:926–9.CrossRefPubMedPubMedCentral
28.
go back to reference Pezzulo AA, Tang XX, Hoegger MJ, Abou Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, Bánfi B, Horswill AR, Stoltz DA, McCray PB Jr, Welsh MJ, Zabner J. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 2012;487(7405):109–113. doi: 10.1038/nature11130. Pezzulo AA, Tang XX, Hoegger MJ, Abou Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, Bánfi B, Horswill AR, Stoltz DA, McCray PB Jr, Welsh MJ, Zabner J. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 2012;487(7405):109–113. doi: 10.​1038/​nature11130.
29.
go back to reference Schwab U, Leigh M, Ribeiro C, Yankaskas J, Burns K, Gilligan P, et al. Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect Immun. 2002;70(8):4547–55.CrossRefPubMedPubMedCentral Schwab U, Leigh M, Ribeiro C, Yankaskas J, Burns K, Gilligan P, et al. Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect Immun. 2002;70(8):4547–55.CrossRefPubMedPubMedCentral
30.
go back to reference Gingues S, Kooi C, Visser MB, Subsin B, Sokol PA. Distribution and expression of the ZmpA metalloprotease in the Burkholderia cepacia complex. J Bacteriol. 2005;187(24):8247–55.CrossRefPubMedPubMedCentral Gingues S, Kooi C, Visser MB, Subsin B, Sokol PA. Distribution and expression of the ZmpA metalloprotease in the Burkholderia cepacia complex. J Bacteriol. 2005;187(24):8247–55.CrossRefPubMedPubMedCentral
31.
go back to reference Conway BA, Chu KK, Bylund J, Altman E, Speert DP. Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell surface interactions and altered bacterial clearance in mice. J Infect Dis. 2004;190:957–66.CrossRefPubMed Conway BA, Chu KK, Bylund J, Altman E, Speert DP. Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell surface interactions and altered bacterial clearance in mice. J Infect Dis. 2004;190:957–66.CrossRefPubMed
32.
go back to reference Silva IN, Ferreira AS, Becker JD, Zlosnik JE, Speert DP, He J, et al. Mucoid morphotype variation of Burkholderia multivorans during chronic cystic fibrosis lung infection is correlated with changes in metabolism, motility, biofilm formation and virulence. Microbiology. 2011;157(Pt 11):3124–37. doi:10.1099/mic.0.050989-0. Silva IN, Ferreira AS, Becker JD, Zlosnik JE, Speert DP, He J, et al. Mucoid morphotype variation of Burkholderia multivorans during chronic cystic fibrosis lung infection is correlated with changes in metabolism, motility, biofilm formation and virulence. Microbiology. 2011;157(Pt 11):3124–37. doi:10.​1099/​mic.​0.​050989-0.
34.
go back to reference Zlosnik JE, Costa PC, Brant R, Hird TJ, Mori PY, Wilcox P, et al. Exopolysaccharide production in BCC and links to clinical outcome. Seattle: International Burkholderia cepacia Working Group; 2010. Abstract 7B Zlosnik JE, Costa PC, Brant R, Hird TJ, Mori PY, Wilcox P, et al. Exopolysaccharide production in BCC and links to clinical outcome. Seattle: International Burkholderia cepacia Working Group; 2010. Abstract 7B
35.
go back to reference Drevinek P, Baldwin A, Lindenburg L, Joshi LT, Marchbank A, Vosahlikova S, et al. Oxidative stress of Burkholderia cenocepacia induces insertion sequence-mediated genomic rearrangements that interfere with macrorestriction-based genotyping. J Clin Microbiol. 2010;48:34–40.CrossRefPubMed Drevinek P, Baldwin A, Lindenburg L, Joshi LT, Marchbank A, Vosahlikova S, et al. Oxidative stress of Burkholderia cenocepacia induces insertion sequence-mediated genomic rearrangements that interfere with macrorestriction-based genotyping. J Clin Microbiol. 2010;48:34–40.CrossRefPubMed
Metadata
Title
Virulence traits associated with Burkholderia cenocepacia ST856 epidemic strain isolated from cystic fibrosis patients
Authors
Milka Malešević
Zorica Vasiljević
Aleksandar Sovtić
Brankica Filipić
Katarina Novović
Milan Kojić
Branko Jovčić
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2017
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-017-0215-y

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