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Journal of Bacteriology, November 2007, p. 7961-7967, Vol. 189, No. 22
0021-9193/07/$08.00+0     doi:10.1128/JB.00789-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Generation of Virulence Factor Variants in Staphylococcus aureus Biofilms{triangledown}

Jeremy M. Yarwood,1* Kara M. Paquette,1 Ilya B. Tikh,1 Esther M. Volper,2 and E. Peter Greenberg3

3M Corporate Research Laboratories, 3M Center, St. Paul, Minnesota 55144,1 Department of Microbiology and W. M. Keck Microbial Communities and Cell Signaling Program, Roy and Lucille Carver College of Medicine, University of Iowa, Iowa City, Iowa 52242,2 Department of Microbiology, University of Washington School of Medicine, Seattle, Washington 981953

Received 21 May 2007/ Accepted 23 July 2007

Several serious diseases are caused by biofilm-associated Staphylococcus aureus. Colonial variants occur in biofilms of other bacterial species, and S. aureus variants are frequently isolated from biofilm-associated infections. Thus, we studied the generation of variants with altered expression of virulence factors in S. aureus biofilms. We observed that the number of variants found in biofilms, as measured by hemolytic activity, varied for different strains. Further study of hemolytic activity and signaling by the accessory gene regulator (Agr) quorum-sensing system in one S. aureus strain revealed three primary biofilm subpopulations: nonhemolytic (Agr deficient), hemolytic (Agr positive), and hyperhemolytic (also Agr positive). The nonhemolytic variant became the numerically dominant subpopulation in the biofilm. The nonhemolytic variant phenotype was stable and heritable, indicating a genetic perturbation, whereas the hyperhemolytic phenotype was unstable, suggesting a phase variation. Transcription profiling revealed that expression of the agr locus and many extracellular virulence factors was repressed in the nonhemolytic variant. Expression of the agr-activating gene, sarU, was also repressed in the nonhemolytic variant, suggesting one potential regulatory pathway responsible for the Agr-deficient phenotype. We suggest that the development of these variants in biofilms may have important clinical implications.

* Corresponding author. Mailing address: 3M Corporate Research Laboratories, 3M Center, Bldg. 201-3E-03, St. Paul, MN 55144. Phone: (651) 737-1033. Fax: (651) 737-5173. E-mail: jyarwood{at}mmm.com

{triangledown} Published ahead of print on 3 August 2007.

Journal of Bacteriology, November 2007, p. 7961-7967, Vol. 189, No. 22
0021-9193/07/$08.00+0     doi:10.1128/JB.00789-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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