Observations of Shear Stress Effects on Staphylococcus aureus Biofilm Formation

Abstract

It is well known that flow plays an important role in the formation, transportation, and dispersion of Staphylococcus aureus biofilms. What was heretofore not known was that the formation of tower structures in these biofilms is strongly shear stress dependent; there is, in fact, a narrow range of shear stresses in which the phenomenon occurs. This work quantifies the observed shear dependence in terms of cell growth, distribution, and fluid mechanics. It represents an important first step in opening up a line of questioning as to the interaction of fluid forces and their influence on the dynamics of tower formation, break-off, and transportation in biofilms by identifying the parameter space in which this phenomenon occurs. We have also introduced state-of-the-art flow measurement techniques to address this problem. Staphylococcus aureus bacteria form biofilms and distinctive microcolony or “tower” structures that facilitate their ability to tolerate antibiotic treatment and to spread within the human body. The formation of microcolonies, which break off, get carried downstream, and serve to initiate biofilms in other parts of the body, is of particular interest here. It is known that flow conditions play a role in the development, dispersion, and propagation of biofilms in general. The influence of flow on microcolony formation and, ultimately, what factors lead to microcolony development are, however, not well understood. The hypothesis being examined is that microcolony structures form within a specific range of levels of shear stress. In this study, laminar shear flow over a range of 0.15 to 1.5 dynes/cm 2 was examined. It was found that microcolony structures form in a narrow range of shear stresses around 0.6 dynes/cm 2 . Further, measurements of cell density as a function of space and time showed that shear dependence can be observed hours before microcolonies form. This is significant because, among other physiologic flows, this is the same shear stress found in large veins in the human vasculature, which, along with catheters of similar diameters and flow rates, may therefore play a critical role in biofilm development and subsequent spreading of infections throughout the body. IMPORTANCE It is well known that flow plays an important role in the formation, transportation, and dispersion of Staphylococcus aureus biofilms. What was heretofore not known was that the formation of tower structures in these biofilms is strongly shear stress dependent; there is, in fact, a narrow range of shear stresses in which the phenomenon occurs. This work quantifies the observed shear dependence in terms of cell growth, distribution, and fluid mechanics. It represents an important first step in opening up a line of questioning as to the interaction of fluid forces and their influence on the dynamics of tower formation, break-off, and transportation in biofilms by identifying the parameter space in which this phenomenon occurs. We have also introduced state-of-the-art flow measurement techniques to address this problem.