Elastic and viscous bond components in the adhesion of colloidal particles and fibrillated streptococci to QCM-D crystal surfaces with different hydrophobicities using Kelvin–Voigt and Maxwell models

Abstract

A quartz-crystal-microbalance with dissipation (QCM-D) can measure molecular mass adsorption as well as register adhesion of colloidal particles. However, analysis of the QCM-D output to quantitatively analyze adhesion of (bio)colloids to obtain viscoelastic bond properties is still a subject of debate. Here, we analyze the QCM-D output to analyze the bond between two hydrophilic streptococcal strains 91 nm long and without fibrillar surface appendages and micron-sized hydrophobic polystyrene particles on QCM-D crystal surfaces with different hydrophobicities, using the Kelvin-Voigt model and the Maxwell model. A Poisson distribution was implemented in order to determine the possible virtues of including polydispersity when fitting model parameters to the data. The quality of the fits did not indicate whether the Kelvin-Voigt or the Maxwell model is preferable and only polydispersity in spring-constants improved the fit for polystyrene particles. The Kelvin-Voigt and Maxwell models both yielded higher spring-constants for the bald streptococcus than for the fibrillated one. In both models, the drag coefficients increased for the bald streptococcus with the ratio of electron-donating over electron-accepting parameters of the crystal surface, while for the fibrillated strain the drag coefficient was similar on all crystal surfaces. Combined with the propensity of fibrillated streptococci to bind to the sensor crystal as a coupled-resonator above the crystal surface, this suggests that the drag experienced by resonator-coupled, hydrophilic particles is more influenced by the viscosity of the bulk water than by interfacial water adjacent to the crystal surface. Hydrophilic particles that lack a surface tether are mass-coupled just above the crystal surface and accordingly probe the drag due to the thin layer of interfacial water that is differently structured on hydrophobic and hydrophilic surfaces. Hydrophobic particles without a surface tether are also mass-coupled, but their drag coefficient decreases when the ratio of electron-donating over electron-accepting parameters increases, suggesting that hydrophobic particles experience less drag due to the structured water adjacent to the surface.

QCM-D characterization of time-dependence of bacterial adhesion

“…For example, Olsson et al (2009) used Streptococcus salivarius mutants that had surface appendages of know length in order to study the effect that fimbriae length had on adhesion over time. “Bald” bacteria demonstrated a frequency decrease, however, more fibrillation led to the adherence of more bacteria which is in agreement with other studies ( Olofsson et al, 2005 , Olsson et al, 2009 , Strauss et al, 2010 , van der Westen et al, 2017 ). It was also found that dissipation was linear when the number of cells was normalized but higher for those with longer fibrils.…”

“…The changes in frequencies can be related directly to changes in mass through the Sauerbrey equation for rigid films and adhesion. However, these models often fall short when trying to directly measure bacterial adhesion due to the complex processes that are involved in bacterial adhesion, as well as coupled resonance ( Tarnapolsky and Freger, 2018 , van der Westen et al, 2017 ). Coupled resonance is most commonly observed when there is a positive shift in frequency is observed unexpectedly when mass is in fact being added to the system.…”

“…Further, if the inertial and spring elastic force of a bacteria on the surface is perfectly balanced, then Δ f will be zero ( Tarnapolsky and Freger, 2018 ). The Voigt-Kelvin extended viscoelastic model corrects the Sauerbrey estimations for higher energy dissipation by adding terms to the Δ f relation to mass and ΔD relation to film rigidity ( Tarnapolsky and Freger, 2018 , van der Westen et al, 2017 ). Analysis of frequency and dissipation changes at different overtones, corresponding to differing penetration depths (250 nm maximum), allows for the study of the effect of fimbriae length or other bacterial surface molecules on adhesion ( Olsson et al, 2009 , Olsson et al, 2010 , Olsson et al, 2011 ), which provides for real-time mechanistic study of the bacterial adhesion process ( Tarnapolsky and Freger, 2018 ).…”

“…Numerous studies demonstrate the power of QCM-D in developing new bacterial adhesion models and studying different stages of biofilm formation. Of particular interest is the ability of the QCM-D to identify time-dependent changes in bacterial attachment and morphological changes ( Contreras et al, 2011 , Eichler et al, 2011 , Feldötö et al, 2008 , Gutman et al, 2013 , Leino et al, 2011 , Marcus et al, 2012 , Olsson et al, 2015 , Olsson et al, 2011 , Otto et al, 1999 , Poitras and Tufenkji, 2009 , Schofield et al, 2007 , Speight and Cooper, 2012 , Sweity et al, 2011 , Tarnapolsky and Freger, 2018 , van der Westen et al, 2017 , Zhou et al, 2000 ). The sensitivity of the QCM-D allows for the detection of changes that happen in seconds or minutes ( Olsson et al, 2010 ), but QCM-D can also be used for very long time scales, even up to days or weeks ( Chen et al, 2010 , Nivens et al, 1993 , Reipa et al, 2006 ).…”

“…Bacterial adhesion to a surface is an extremely complex process that begins with: 1) extracellular and intracellular signaling to either recognize a surface or recruit other bacteria to the surface ( Khelissa et al, 2017 , Tarnapolsky and Freger, 2018 ), 2) reversible adhesion to the surface via surface proteins such as fibrils and lipopolysaccharide (LPS) ( Goulter et al, 2009 , Kostakioti et al, 2013 ), 3) irreversible adhesion to the surface, 4) Extracellular matrix (ECM) production and growth of the biofilm changes in protein synthesis and morphological changes ( Goulter et al, 2009 , Khelissa et al, 2017 , Kostakioti et al, 2013 ) and 5) maturation of the biofilm and dispersion ( Flemming et al, 2016 , Gutman et al, 2013 , Kwon et al, 2006 , Römling et al, 2014 , Tandogan et al, 2017 , Tuson and Weibel, 2013 , van der Westen et al, 2017 ).…”