Evaluation of the ability of C. albicans to form biofilm in the presence of phage-resistant phenotypes of P. aeruginosa

Pseudomonas aeruginosa and Candida albicans are disparate microbial species, but both are known to be opportunistic pathogens frequently associated with nosocomial infections. The aim of this study was to provide a better understanding of the interactions between these microorganisms in dual-species biofilms. Several bacteriophage-resistant P. aeruginosa phenotypes have been isolated and were used in dual-species mixed-biofilm studies. Twenty-four and 48 h mixed-biofilms were formed using the isolated phenotypes of phage-resistant P. aeruginosa and these were compared with similar experiments using other P. aeruginosa strains with a defined lipopolysaccharide (LPS) deficiency based on chromosomal knockout of specific LPS biosynthetic genes. Overall, the results showed that the variants of phage-resistant P. aeruginosa and LPS mutants were both less effective in inhibiting the growth of C. albicans in mixed-biofilms compared to the wild-type strains of P. aeruginosa. Conversely, the proliferation of P. aeruginosa was not influenced by the presence of C. albicans. In conclusion, the ability of strains of P. aeruginosa to inhibit the formation of a biofilm of C. albicans appears to be correlated with the LPS chain lengths of phenotypes of P. aeruginosa, suggesting that LPS has a suppressive effect on the growth of C. albicans.

[1]  L. Samaranayake,et al.  Pseudomonas aeruginosa lipopolysaccharide inhibits Candida albicans hyphae formation and alters gene expression during biofilm development. , 2013, Molecular oral microbiology.

[2]  Jungmin Kim,et al.  Pseudomonas aeruginosa Bacteriophage PA1Ø Requires Type IV Pili for Infection and Shows Broad Bactericidal and Biofilm Removal Activities , 2012, Applied and Environmental Microbiology.

[3]  S. Sillankorva,et al.  Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. , 2011, Research in microbiology.

[4]  C. Fernandez-Prada,et al.  Bacteriophage-Resistant Mutants in Yersinia pestis: Identification of Phage Receptors and Attenuation for Mice , 2011, PloS one.

[5]  S. de Bentzmann,et al.  The Pseudomonas aeruginosa opportunistic pathogen and human infections. , 2011, Environmental microbiology.

[6]  J. Lam,et al.  Genetic and Functional Diversity of Pseudomonas aeruginosa Lipopolysaccharide , 2011, Front. Microbio..

[7]  R. Lavigne,et al.  Phenotypic and genotypic variations within a single bacteriophage species , 2011, Virology Journal.

[8]  R M Watt,et al.  Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. , 2010, Journal of medical microbiology.

[9]  G. Butler,et al.  Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans. , 2010, Microbiology.

[10]  R. Watt,et al.  Pseudomonas aeruginosa inhibits in-vitro Candida biofilm development , 2010, BMC Microbiology.

[11]  David W Williams,et al.  In Vitro Biofilm Activity of Non-Candida albicansCandida Species , 2010, Current Microbiology.

[12]  L. Samaranayake,et al.  Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation. , 2009, Journal of medical microbiology.

[13]  David W Williams,et al.  Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. , 2009, Medical mycology.

[14]  S. Nseir,et al.  Pseudomonas aeruginosa and Candida albicans: do they really need to stick together? , 2009, Critical care medicine.

[15]  R. Donlan.  Preventing biofilms of clinically relevant organisms using bacteriophage. , 2009, Trends in microbiology.

[16]  P. Neubauer,et al.  Pseudomonas fluorescens biofilms subjected to phage phiIBB-PF7A , 2008, BMC biotechnology.

[17]  F. O'Gara,et al.  Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. , 2008, Journal of medical microbiology.

[18]  C. van Delden,et al.  Pseudomonas aeruginosa bloodstream infections: how should we treat them? , 2007, International journal of antimicrobial agents.

[19]  G. Hanlon,et al.  Bacteriophages: an appraisal of their role in the treatment of bacterial infections. , 2007, International journal of antimicrobial agents.

[20]  J. Fralick,et al.  Phage Therapy of Pseudomonas aeruginosa Infection in a Mouse Burn Wound Model , 2007, Antimicrobial Agents and Chemotherapy.

[21]  D. Hogan,et al.  Fungal--bacterial interactions: a mixed bag of mingling microbes. , 2006, Current opinion in microbiology.

[22]  R. Donlan,et al.  Using Bacteriophages To Reduce Formation of Catheter-Associated Biofilms by Staphylococcus epidermidis , 2006, Antimicrobial Agents and Chemotherapy.

[23]  G. Pierce.  Pseudomonas aeruginosa, Candida albicans, and device-related nosocomial infections: implications, trends, and potential approaches for control , 2005, Journal of Industrial Microbiology and Biotechnology.

[24]  R. Kolter,et al.  A Pseudomonas aeruginosa quorum‐sensing molecule influences Candida albicans morphology , 2004, Molecular microbiology.

[25]  A. Górski,et al.  Bacteriophages as an efficient therapy for antibiotic-resistant septicemia in man. , 2003, Transplantation proceedings.

[26]  R. Kolter,et al.  Pseudomonas-Candida Interactions: An Ecological Role for Virulence Factors , 2002, Science.

[27]  K. Tait,et al.  The efficacy of bacteriophage as a method of biofilm eradication , 2002 .

[28]  R. Calderone,et al.  Virulence factors of Candida albicans. , 2001, Trends in microbiology.

[29]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[30]  L. Burrows,et al.  Involvement of the rml locus in core oligosaccharide and O polysaccharide assembly in Pseudomonas aeruginosa. , 2000, Microbiology.

[31]  J. Lam,et al.  Synthesis of the A‐band polysaccharide sugar D‐rhamnose requires Rmd and WbpW: identification of multiple AlgA homologues, WbpW and ORF488, in Pseudomonas aeruginosa , 1998, Molecular microbiology.

[32]  C. Nombela,et al.  Candida albicans: genetics, dimorphism and pathogenicity. , 1998, International microbiology : the official journal of the Spanish Society for Microbiology.

[33]  L. Burrows,et al.  Three rhamnosyltransferases responsible for assembly of the A‐band D‐rhamnan polysaccharide in Pseudomonas aeruginosa: a fourth transferase, WbpL, is required for the initiation of both A‐band and B‐band lipopolysaccharide synthesis , 1998, Molecular microbiology.

[34]  J. Lam,et al.  Identification and functional characterization of an ABC transport system involved in polysaccharide export of A-band lipopolysaccharide in Pseudomonas aeruginosa , 1997, Journal of bacteriology.

[35]  J. Lam,et al.  Diverse VH and V kappa genes encode antibodies to Pseudomonas aeruginosa LPS. , 1995, Journal of immunology.

[36]  H. Schweizer,et al.  Molecular cloning and characterization of the rfc gene of Pseudomonas aeruginosa (serotype O5) , 1995, Molecular microbiology.

[37]  C. Galanos,et al.  Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels , 1990, Journal of clinical microbiology.

[38]  P. Hitchcock,et al.  Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels , 1983, Journal of bacteriology.

[39]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[40]  M. Kollef,et al.  The Epidemiology, Pathogenesis and Treatment of Pseudomonas aeruginosa Infections , 2012, Drugs.

[41]  Sudhir Aggarwal,et al.  Urinary tract infections caused by Pseudomonas aeruginosa: a minireview. , 2009, Journal of infection and public health.

[42]  A. Kropinski.  Measurement of the bacteriophage inactivation kinetics with purified receptors. , 2009, Methods in molecular biology.

[43]  E. Lingohr,et al.  Enumeration of bacteriophages by double agar overlay plaque assay. , 2009, Methods in molecular biology.

[44]  E. Lingohr,et al.  Enumeration of bacteriophages using the small drop plaque assay system. , 2009, Methods in molecular biology.

[45]  Toshikazu Tani,et al.  Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases , 2005, Journal of infection and chemotherapy : official journal of the Japan Society of Chemotherapy.

[46]  A. Górski,et al.  Bacteriophage therapy for infections in cancer patients , 2001 .

[47]  B. Iglewski,et al.  Cell-to-cell signaling and Pseudomonas aeruginosa infections. , 1998, Emerging infectious diseases.

[48]  A. Wright,et al.  Lipopolysaccharide as a Bacteriophage Receptor , 1980 .