Viscoelastic properties of <i>Staphylococcus aureus</i> and <i>Staphylococcus epidermidis</i> mono‐microbial biofilms

Stefano, Antonio Di; D’Aurizio, Eleonora; Trubiani, Oriana; Grande, Rossella; Campli, Emanuela Di; Giulio, Mara Di; Bartolomeo, Soraya Di; Sozio, Piera; Iannitelli, Antonio; Nostro, Antonia; Cellini, Luigina

doi:10.1111/j.1751-7915.2009.00120.x

Cited by 48 publications

(55 citation statements)

References 33 publications

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“…This suggests that during phase transition from levan particles to levan aggregates, the material changed from a primarily viscous fluid to a viscoelastic fluid. The formation of a viscoelastic matrix during biofilm formation is another hallmark of the biofilm matrix (34)(35)(36). The results therefore indicate that DNA is able to induce transition in levan from low viscosity in pure solution to viscoelastic material in levan-DNA mixtures.…”

Section: Discussionmentioning

confidence: 86%

Viscoelastic Properties of Levan-DNA Mixtures Important in Microbial Biofilm Formation as Determined by Micro- and Macrorheology

Stojković

Sretenovic

Dogša

et al. 2015

Biophysical Journal

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We studied the viscoelastic properties of homogeneous and inhomogeneous levan-DNA mixtures using optical tweezers and a rotational rheometer. Levan and DNA are important components of the extracellular matrix of bacterial biofilms. Their viscoelastic properties influence the mechanical as well as molecular-transport properties of biofilm. Both macro- and microrheology measurements in homogeneous levan-DNA mixtures revealed pseudoplastic behavior. When the concentration of DNA reached a critical value, levan started to aggregate, forming clusters of a few microns in size. Microrheology using optical tweezers enabled us to measure local viscoelastic properties within the clusters as well as in the DNA phase surrounding the levan aggregates. In phase-separated levan-DNA mixtures, the results of macro- and microrheology differed significantly. The local viscosity and elasticity of levan increased, whereas the local viscosity of DNA decreased. On the other hand, the results of bulk viscosity measurements suggest that levan clusters do not interact strongly with DNA. Upon treatment with DNase, levan aggregates dispersed. These results demonstrate the advantages of microrheological measurements compared to bulk viscoelastic measurements when the materials under investigation are complex and inhomogeneous, as is often the case in biological samples.

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Section: Discussionmentioning

confidence: 86%

Viscoelastic Properties of Levan-DNA Mixtures Important in Microbial Biofilm Formation as Determined by Micro- and Macrorheology

Stojković

Sretenovic

Dogša

et al. 2015

Biophysical Journal

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“…Although many viscometric measurements have been made for biofilms grown on solid substrates (6,24,25), the mechanical properties of biofilms formed at air-liquid interfaces are comparatively less well characterized. We expect the two types of biofilm to have very different viscosities.…”

Section: Resultsmentioning

confidence: 99%

Bacillus subtilis spreads by surfing on waves of surfactant

Angelini

Roper

Kolter

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

167

122

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The bacterium Bacillus subtilis produces the molecule surfactin, which is known to enhance the spreading of multicellular colonies on nutrient substrates by lowering the surface tension of the surrounding fluid, and to aid in the formation of aerial structures. Here we present experiments and a mathematical model that demonstrate how the differential accumulation rates induced by the geometry of the bacterial film give rise to surfactant waves. The spreading flux increases with increasing biofilm viscosity. Community associations are known to protect bacterial populations from environmental challenges such as predation, heat, or chemical stresses, and enable digestion of a broader range of nutritive sources. This study provides evidence of enhanced dispersal through cooperative motility, and points to nonintuitive methods for controlling the spread of biofilms.biofilms | thin-film hydrodynamics B acteria bind to surfaces and to liquid-air interfaces to form biofilms, thick mats of cells cemented together by exopolysaccharides. Biofilms endow pathogenic bacteria with enhanced virulence and resistance to antibiotics. Although many recent studies have focused on the adhesins that bind bacteria to each other and to abiotic substrates (1-3) and on the signaling pathways that initiate biofilm growth (4, 5), very little is known about the physical processes by which these colonies spread over or between nutrient sources. Previous studies have highlighted the role of individual cell motility and of passive processes such as the advection of cell aggregates in propagating biofilms (6), but such propagative mechanisms depend on dispersive fluid flows. In addition to being implicated in the development of aerial structures (7), in antagonistic interactions between colonies of different bacterial species (8) the biosurfactant surfactin is known to be necessary for the spreading of colonies of Bacillus subtilis in the absence of external fluid flows (9, 10). However, the physical consequences of the surfactant-like behavior of surfactin on the spreading of biofilms remains unknown.Here we show that gradients in the concentration of surfactin by cells in a liquid pellicle generates surface-tension gradients that drive cooperative spreading. The essential mechanism of surface-tension gradient-driven spreading is similar to the forced spreading of a thin film due to surface-tension gradients induced by temperature gradients (11,12) or by exogenous surfactants (13,14).In the present context, a surface-tension gradient develops because of the geometry of the bacterial biofilm: The bacterial pellicle is thinner at the edge than at the center. The surfactin produced by every cell moves rapidly to the air-fluid film interface, locally reducing the surface tension. Assuming the surfactin production rate is identical for each cell, the concentration of surfactant is greater at the center of the pellicle than at the edge, which results in a gradient in surface tension that drags the film outward, away from the center of the pellicle. T...

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“…The constituent components of EPS altogether compose up to 50–90% of the total organic matter in biofilms [93] and create a highly hydrated viscoelastic gel [94] that provides increased flexibility to cope with environmental stresses [95, 96]. In particular, due to inherent characteristics of viscoelasticity, biofilms exhibit enhanced mechanical stability against fragmentation by shear flows [97].…”

Section: Rheology Of Biofilmsmentioning

confidence: 99%

“…The associated creep curves typically display five characteristic regions (see Fig. 4(b)): (1) an immediate elastic deformation, (2) a transient, nonlinear viscoelastic response, (3) a steady-state viscous flow with constant viscosity, (4) an instantaneous partial elastic recoil upon removal of shear stress, and (5) a residual deformation due to fluid-like behavior [95, 98, 100]. When shear stresses larger than a certain threshold, referred to as the yield point, are applied, the biofilm flows entirely analogously to a liquid [101] and the biofilm stiffness drops by several orders of magnitude [102].…”

Section: Rheology Of Biofilmsmentioning

confidence: 99%

Interplay of physical mechanisms and biofilm processes: review of microfluidic methods

et al. 2015

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Bacteria in natural and artificial environments often reside in self-organized, integrated communities known as biofilms. Biofilms are highly structured entities consisting of bacterial cells embedded in a matrix of self-produced extracellular polymeric substances (EPS). The EPS matrix acts like a biological ‘glue’ enabling microbes to adhere to and colonize a wide range of surfaces. Once integrated into biofilms, bacterial cells can withstand various forms of stress such as antibiotics, hydrodynamic shear and other environmental challenges. Because of this, biofilms of pathogenic bacteria can be a significant health hazard often leading to recurrent infections. Biofilms can also lead to clogging and material degradation; on the other hand they are an integral part of various environmental processes such as carbon sequestration and nitrogen cycles. There are several determinants of biofilm morphology and dynamics, including the genotypic and phenotypic states of constituent cells and various environmental conditions. Here, we present an overview of the role of relevant physical processes in biofilm formation, including propulsion mechanisms, hydrodynamic effects, and transport of quorum sensing signals. We also provide a survey of microfluidic techniques utilized to unravel the associated physical mechanisms. Further, we discuss the future research areas for exploring new ways to extend the scope of the microfluidic approach in biofilm studies.

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Viscoelastic properties of Staphylococcus aureus and Staphylococcus epidermidis mono‐microbial biofilms

Cited by 48 publications

References 33 publications

Viscoelastic Properties of Levan-DNA Mixtures Important in Microbial Biofilm Formation as Determined by Micro- and Macrorheology

Viscoelastic Properties of Levan-DNA Mixtures Important in Microbial Biofilm Formation as Determined by Micro- and Macrorheology

Bacillus subtilis spreads by surfing on waves of surfactant

Interplay of physical mechanisms and biofilm processes: review of microfluidic methods

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