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Infection and Immunity, September 2009, p. 3978-3991, Vol. 77, No. 9
0019-9567/09/$08.00+0 doi:10.1128/IAI.00616-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
Relevant Role of Fibronectin-Binding Proteins in Staphylococcus aureus Biofilm-Associated Foreign-Body Infections
,
Marta Vergara-Irigaray,1
Jaione Valle,1
Nekane Merino,1
Cristina Latasa,1
Begoña García,1
Igor Ruiz de los Mozos,1
Cristina Solano,1
Alejandro Toledo-Arana,1
José R. Penadés,2 and
Iñigo Lasa1*
Laboratory of Microbial Biofilms, Instituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de Navarra, 31006 Pamplona, Spain,1 Centro de Investigación y Tecnología Animal, Instituto Valenciano de Investigaciones Agrarias (CITA-IVIA), Apdo 187, 12400 Segorbe, Castellón, Spain2
Received 31 May 2009/ Returned for modification 15 June 2009/ Accepted 24 June 2009
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.
* Corresponding author. Mailing address: Instituto de Agrobiotecnología, Universidad Pública de Navarra, Pamplona-31006, Spain. Phone: 34 948 168007. Fax: 34 948 232191. E-mail: ilasa{at}unavarra.es
Published ahead of print on 6 July 2009.
Supplemental material for this article may be found at http://iai.asm.org/.
Infection and Immunity, September 2009, p. 3978-3991, Vol. 77, No. 9
0019-9567/09/$08.00+0 doi:10.1128/IAI.00616-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
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