Viscoelastic fluid description of bacterial biofilm material properties

Abstract

A mathematical model describing the constitutive properties of biofilms is required for predicting biofilm deformation, failure, and detachment in response to mechanical forces. Laboratory observations indicate that biofilms are viscoelastic materials. Likewise, current knowledge of biofilm internal structure suggests modeling biofilms as associated polymer viscoelastic systems. Supporting experimental results and a system of viscoelastic fluid equations with a linear Jeffreys viscoelastic stress-strain law are presented here. This system of equations is based on elements of associated polymer physics and is also consistent with presented and previous experimental results. A number of predictions can be made. One particularly interesting result is the prediction of an elastic relaxation time on the order of a few minutes-biofilm disturbances on shorter time scales produce an elastic response, biofilm disturbances on longer time scales result in viscous flow, i.e., nonreversible biofilm deformation. Although not previously recognized, evidence of this phenomenon is in fact present in recent experimental results.

Bacterial swimmers that infiltrate and take over the biofilm matrix

“…Bacteria moved up to 16 μm/s in all directions, following different paths through the biofilm mass. Swimming cells passing through the bulk of the biofilm created transient tunnels that lasted for about 2-5 s, highlighting the reversible elastic properties of the matrix (1,12). In addition to linear movement, rapid circular movements of bacterial chains generated local dispersion and large transient pores (∼10 μm diameter), as visible in the still frame from Movie S1 (Fig.…”

“…However, strains of motile species Pseudomonas aeruginosa (ATCC 1592) and Bacillus subtilis (168) did not detectably irrigate their own biofilms in our test conditions. Swimming in such biostructures might require sufficient kinetic energy to overcome the cohesive force generated by the EPS, and would thus vary according to the "swimmer" and the target biofilm (1,11,12). It is also possible that biofilm bacteria modulate stealth swimmer activity via signaling molecules that inhibit motility within the matrix.…”

“…Above a critical kinetic energy specific to each matrix, a motile swimmer can generate a reversible transient elastic response and/or an irreversible deformation (1,12). We therefore tested the capacity of motile B. thuringiensis 407 to tunnel into biofilms comprising different Gram-positive or Gramnegative pathogens (Table S1): Staphylococcus aureus RN4220 (Movie S5), Enterococcus faecalis (ATCC 700802; as shown in Movie S6), Y. enterocolitica (CIP 81.41), P. aeruginosa (ATCC 1592), or Listeria monocytogenes (ATCC BAA-679).…”

A microfluidic method and custom model for continuous, non-intrusive biofilm viscosity measurements under different nutrient conditions

“…For example, shear thinning has been reported for some strains such as Streptococcus mutans and Chlorella vulgaris 7,54,57 and shear thickening in P. aeruginosa. 19 Reported mechanical responses to different ions have also been varied. 20,23,36 Moreover, living biofilms demonstrate intriguing time-dependent behaviour.…”

“…For example, parallel plate rheometers 36 or analysis of stress-strain curves produced using time-limited changes to shear forces by cycling nutrient flow rates in growth cells. 11,19,45,51,52 However, changes to imposed shear can induce measurement biases in viscosity for non-Newtonian biofilms. Moreover, since the time-scale of most laboratory growth experiments is longer than the elastic relaxation time quoted above, biofilms exhibit viscous liquid properties.…”