An 18 kDa scaffold protein is critical for Staphylococcus epidermidis biofilm formation

Rahel Decker; Christoph Burdelski; Melanie Zobiak; Henning Büttner; Gefion Franke; Martin Christner; Katharina Saß; Bernd Zobiak; Hanae A Henke; Alexander R Horswill; Markus Bischoff; Stephanie Bur; Torsten Hartmann; Carolyn R Schaeffer; Paul D Fey; Holger Rohde

doi:10.1371/journal.ppat.1004735

An 18 kDa scaffold protein is critical for Staphylococcus epidermidis biofilm formation

PLoS Pathog. 2015 Mar 23;11(3):e1004735. doi: 10.1371/journal.ppat.1004735. eCollection 2015 Mar.

Authors

Rahel Decker¹, Christoph Burdelski¹, Melanie Zobiak¹, Henning Büttner¹, Gefion Franke¹, Martin Christner¹, Katharina Saß¹, Bernd Zobiak², Hanae A Henke¹, Alexander R Horswill³, Markus Bischoff⁴, Stephanie Bur⁴, Torsten Hartmann⁴, Carolyn R Schaeffer⁵, Paul D Fey⁵, Holger Rohde¹

Affiliations

¹ Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Hamburg, Germany.
² UKE Microscopy Imaging Facility, Universitätsklinikum Hamburg-Eppendorf, Hamburg, Germany.
³ Department of Microbiology, Carver College of Medicine, University of Iowa, Iowa City, Iowa, United States of America.
⁴ Institut für Medizinische Mikrobiologie und Hygiene, Universitätsklinikum des Saarlandes, Homburg, Germany.
⁵ Department of Pathology and Microbiology, Center for Staphylococcal Research, University of Nebraska Medical Center, Omaha, Nebraska, United States of America.

Abstract

Virulence of the nosocomial pathogen Staphylococcus epidermidis is crucially linked to formation of adherent biofilms on artificial surfaces. Biofilm assembly is significantly fostered by production of a bacteria derived extracellular matrix. However, the matrix composition, spatial organization, and relevance of specific molecular interactions for integration of bacterial cells into the multilayered biofilm community are not fully understood. Here we report on the function of novel 18 kDa Small basic protein (Sbp) that was isolated from S. epidermidis biofilm matrix preparations by an affinity chromatographic approach. Sbp accumulates within the biofilm matrix, being preferentially deposited at the biofilm-substratum interface. Analysis of Sbp-negative S. epidermidis mutants demonstrated the importance of Sbp for sustained colonization of abiotic surfaces, but also epithelial cells. In addition, Sbp promotes assembly of S. epidermidis cell aggregates and establishment of multilayered biofilms by influencing polysaccharide intercellular-adhesin (PIA) and accumulation associated protein (Aap) mediated intercellular aggregation. While inactivation of Sbp indirectly resulted in reduced PIA-synthesis and biofilm formation, Sbp serves as an essential ligand during Aap domain-B mediated biofilm accumulation. Our data support the conclusion that Sbp serves as an S. epidermidis biofilm scaffold protein that significantly contributes to key steps of surface colonization. Sbp-negative S. epidermidis mutants showed no attenuated virulence in a mouse catheter infection model. Nevertheless, the high prevalence of sbp in commensal and invasive S. epidermidis populations suggests that Sbp plays a significant role as a co-factor during both multi-factorial commensal colonization and infection of artificial surfaces.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bacterial Adhesion / physiology*
Biofilms / growth & development*
Mice
Periplasmic Binding Proteins / genetics
Periplasmic Binding Proteins / metabolism*
Staphylococcus epidermidis / physiology*

Substances

Periplasmic Binding Proteins
sulfate-binding protein, bacteria

Grants and funding

This work was supported by the Deutsche Forschungsgemeinschaft http://www.dfg.de/; grants Ro2413/3-1, given to H.R.; Bi1350/1-1, given to M.B.) and the Bundesministerium für Bildung und Forschung http://www.genomik-transfer.de/; grant 0315587C, given to H.R.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.