Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms

Medora J. Huseby, Andrew C. Kruse, Jeff Digre, Petra L. Kohler, Jillian A. Vocke, Ethan E. Mann, Kenneth W Bayles, Gregory A. Bohach, Patrick M. Schlievert, Douglas H. Ohlendorf, Cathleen A. Earhart

Research output: Contribution to journalArticle

92 Citations (Scopus)

Abstract

Biofilms are surface-associated communities of microbes encompassed by an extracellular matrix. It is estimated that 80% of all bacterial infections involve biofilm formation, but the structure and regulation of biofilms are incompletely understood. Extracellular DNA (eDNA) is a major structural component in many biofilms of the pathogenic bacterium Staphylococcus aureus, but its role is enigmatic. Here, we demonstrate that beta toxin, a neutral sphingomyelinase and a virulence factor of S. aureus, forms covalent cross-links to itself in the presence of DNA (we refer to this as biofilm ligase activity, independent of sphingomyelinase activity) producing an insoluble nucleoprotein matrix in vitro. Furthermore, we show that beta toxin strongly stimulates biofilm formation in vivo as demonstrated by a role in causation of infectious endocarditis in a rabbit model. Together, these results suggest that beta toxin cross-linking in the presence of eDNA assists in forming the skeletal framework upon which staphylococcal biofilms are established.

Original languageEnglish (US)
Pages (from-to)14407-14412
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number32
DOIs
StatePublished - Aug 10 2010

Fingerprint

Nucleoproteins
Biofilms
Sphingomyelin Phosphodiesterase
Staphylococcus aureus
DNA
Virulence Factors
Ligases
Endocarditis
Bacterial Infections
Causality
Extracellular Matrix
Rabbits
Bacteria

Keywords

  • Exotoxins
  • Staphyloccus aureus
  • Virulence

ASJC Scopus subject areas

  • General

Cite this

Huseby, M. J., Kruse, A. C., Digre, J., Kohler, P. L., Vocke, J. A., Mann, E. E., ... Earhart, C. A. (2010). Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. Proceedings of the National Academy of Sciences of the United States of America, 107(32), 14407-14412. https://doi.org/10.1073/pnas.0911032107

Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. / Huseby, Medora J.; Kruse, Andrew C.; Digre, Jeff; Kohler, Petra L.; Vocke, Jillian A.; Mann, Ethan E.; Bayles, Kenneth W; Bohach, Gregory A.; Schlievert, Patrick M.; Ohlendorf, Douglas H.; Earhart, Cathleen A.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 32, 10.08.2010, p. 14407-14412.

Research output: Contribution to journalArticle

Huseby, MJ, Kruse, AC, Digre, J, Kohler, PL, Vocke, JA, Mann, EE, Bayles, KW, Bohach, GA, Schlievert, PM, Ohlendorf, DH & Earhart, CA 2010, 'Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms', Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 32, pp. 14407-14412. https://doi.org/10.1073/pnas.0911032107
Huseby, Medora J. ; Kruse, Andrew C. ; Digre, Jeff ; Kohler, Petra L. ; Vocke, Jillian A. ; Mann, Ethan E. ; Bayles, Kenneth W ; Bohach, Gregory A. ; Schlievert, Patrick M. ; Ohlendorf, Douglas H. ; Earhart, Cathleen A. / Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. In: Proceedings of the National Academy of Sciences of the United States of America. 2010 ; Vol. 107, No. 32. pp. 14407-14412.
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