Relevant Role of Fibronectin-Binding Proteins in Staphylococcus aureus Biofilm-Associated Foreign-Body Infections

• Published in: Infection and Immunity Vol. 77; no. 9; pp. 3978 - 3991
• Main Authors: Vergara-Irigaray, Marta, Valle, Jaione, Merino, Nekane, Latasa, Cristina, García, Begoña, Ruiz de los Mozos, Igor, Solano, Cristina, Toledo-Arana, Alejandro, Penadés, José R, Lasa, Iñigo
• Format: Journal Article
• Language: English
• Published: Washington, DC American Society for Microbiology 01.09.2009; American Society for Microbiology (ASM)
• Subjects: Acetylglucosamine; Acetylglucosamine - physiology; Adhesins; Adhesins, Bacterial; Adhesins, Bacterial - physiology; bacteria; Bacterial Proteins; Bacterial Proteins - physiology; Bacteriology; biofilm; Biofilms; Biological and medical sciences; Catheter-Related Infections; Catheter-Related Infections - etiology; Catheters; Chronic infection; Colonization; Environmental conditions; etiology; Extracellular matrix; Fibronectin-binding protein; Fundamental and applied biological sciences. Psychology; gene overexpression; Humans; medical equipment; Methicillin; Microbiology; Miscellaneous; Molecular Pathogenesis; mutants; Osmotic stress; phenotype; physiology; Plasmids; Polysaccharides; Polysaccharides, Bacterial; Polysaccharides, Bacterial - physiology; protein families; Scanning electron microscopy; SOS response; SOS Response (Genetics); Soybeans; Staphylococcal Infections; Staphylococcal Infections - etiology; Staphylococcus aureus; Staphylococcus aureus - physiology; surface proteins; Trans-Activators; Trans-Activators - physiology; Binding protein; Microbiology; Biofilm; Bacteria; Micrococcales; Micrococcaceae; Foreign body; Immunity; Fibronectin; Staphylococcus aureus
• ISSN: 0019-9567; 1098-5522; 1098-5522
• DOI: 10.1128/IAI.00616-09

Staphylococcus aureus can establish chronic infections on implanted medical devices due to its capacity to form biofilms. Analysis of the factors that assemble cells into a biofilm has revealed the occurrence of strains that produce either a polysaccharide intercellular adhesin/poly-N-acetylglucosamine (PIA/PNAG) exopolysaccharide- or a protein-dependent biofilm. Examination of the influence of matrix nature on the biofilm capacities of embedded bacteria has remained elusive, because a natural strain that readily converts between a polysaccharide- and a protein-based biofilm has not been studied. Here, we have investigated the clinical methicillin (meticillin)-resistant Staphylococcus aureus strain 132, which is able to alternate between a proteinaceous and an exopolysaccharidic biofilm matrix, depending on environmental conditions. Systematic disruption of each member of the LPXTG surface protein family identified fibronectin-binding proteins (FnBPs) as components of a proteinaceous biofilm formed in Trypticase soy broth-glucose, whereas a PIA/PNAG-dependent biofilm was produced under osmotic stress conditions. The induction of FnBP levels due to a spontaneous agr deficiency present in strain 132 and the activation of a LexA-dependent SOS response or FnBP overexpression from a multicopy plasmid enhanced biofilm development, suggesting a direct relationship between the FnBP levels and the strength of the multicellular phenotype. Scanning electron microscopy revealed that cells growing in the FnBP-mediated biofilm formed highly dense aggregates without any detectable extracellular matrix, whereas cells in a PIA/PNAG-dependent biofilm were embedded in an abundant extracellular material. Finally, studies of the contribution of each type of biofilm matrix to subcutaneous catheter colonization revealed that an FnBP mutant displayed a significantly lower capacity to develop biofilm on implanted catheters than the isogenic PIA/PNAG-deficient mutant.