Towards standardized mechanical characterization of microbial biofilms: analysis and critical review

Boudarel, Héloïse; Mathias, Jean‐Denis; Blaysat, Benoît; Grédiac, Michel

doi:10.1038/s41522-018-0062-5

Cited by 124 publications

(94 citation statements)

References 132 publications

(171 reference statements)

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“…While our study uses biofilm grown on agar plates which is an artificial system, in reality biofilms within natural environments are subjected to shear forces, varying amounts of hydration (water content), temperature and various other factors. Many of these factors including a variety of tools have confounded rheological measurements of biofilms in the past 84 , as describing the rheological state of a biofilm (akin to colloids) remains a challenging proposition. Part of the problem can be attributed to the active nature of biofilms.…”

Section: Discussionmentioning

confidence: 99%

Nonlinear rheological characteristics of single species bacterial biofilms

Jana

Charlton

Eland

et al. 2020

npj Biofilms Microbiomes

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Bacterial biofilms in natural and artificial environments perform a wide array of beneficial or detrimental functions and exhibit resistance to physical as well as chemical perturbations. In dynamic environments, where periodic or aperiodic flows over surfaces are involved, biofilms can be subjected to large shear forces. The ability to withstand these forces, which is often attributed to the resilience of the extracellular matrix. This attribute of the extracellular matrix is referred to as viscoelasticity and is a result of selfassembly and cross-linking of multiple polymeric components that are secreted by the microbes. We aim to understand the viscoelastic characteristic of biofilms subjected to large shear forces by performing Large Amplitude Oscillatory Shear (LAOS) experiments on four species of bacterial biofilms: Bacillus subtilis, Comamonas denitrificans, Pseudomonas fluorescens and Pseudomonas aeruginosa. We find that nonlinear viscoelastic measures such as intracycle strain stiffening and intracycle shear thickening for each of the tested species, exhibit subtle or distinct differences in the plot of strain amplitude versus frequency (Pipkin diagram). The biofilms also exhibit variability in the onset of nonlinear behaviour and energy dissipation characteristics, which could be a result of heterogeneity of the extracellular matrix constituents of the different biofilms. The results provide insight into the nonlinear rheological behaviour of biofilms as they are subjected to large strains or strain rates; a situation that is commonly encountered in nature, but rarely investigated.

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Section: Discussionmentioning

confidence: 99%

Nonlinear rheological characteristics of single species bacterial biofilms

Jana

Charlton

Eland

et al. 2020

npj Biofilms Microbiomes

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“…In this work, we developed a novel membrane-based microfluidic device that we named the extensive microperfusion system (EMPS), which can realize a uniformly controlled environment for wide-area observations of microbes. We believe that the EMPS has potential applications in a wide range of problems with dense cellular populations, including living active matter systems ( Bär et al (2019) ; Be’er and Ariel (2019) ) and biofilm growth ( Hall-Stoodley et al (2004) ; Boudarel et al (2018) ; Fuqua et al (2019) ). Here we focused on statistical characterizations of single cell morphology during the reductive division of E. coli .…”

Section: Resultsmentioning

confidence: 99%

Scale invariance during bacterial reductive division observed by an extensive microperfusion system

Shimaya

Okura

Wakamoto

et al. 2020

Preprint

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In stable environments, cell size fluctuations are thought to be governed by simple 9 physical principles, as suggested by recent finding of scaling properties. Here we show, using E. coli, 10 that the scaling concept also rules cell size fluctuations under time-dependent conditions, even 11 though the distribution changes with time. We develop a microfluidic device for observing dense 12 and large bacterial populations, under uniform and switchable conditions. Triggering bacterial 13 reductive division by switching to non-nutritious medium, we find that the cell size distribution 14 changes in a specific manner that keeps its normalized form unchanged; in other words, scale 15 invariance holds. This finding is underpinned by simulations of a model based on cell growth and 16 intracellular replication. We also formulate the problem theoretically and propose a sufficient 17 condition for the scale invariance. Our results emphasize the importance of intrinsic cellular 18 replication processes in this problem, suggesting different distribution trends for bacteria and 19 eukaryotes. 20 21 Biswas et al. (2014a)), have been obtained under steady environments, for which our understanding 37 of single-cell growth statistics has also been significantly deepened recently (Ho et al. (2018); Jun 38 et al. (2018); Cadart et al. (2019)). By contrast, it is unclear whether such a simple concept as 39 1 of 25 Manuscript submitted to eLife scale invariance is valid under time-dependent conditions, where different regulations of cell cycle 40 kinetics may come into play in response to environmental variations. In particular, when bacterial 41 cells enter the stationary phase from the exponential growth phase, they undergo reductive division, 42 during which both the typical cell size and the amount of DNA per cell decrease (Nyström (2004); 43 Kaprelyants and Kell (1993); Arias et al. (2012); Gray et al. (2019)). Although this behavior itself is 44 commonly observed in test tube cultivation, little is known about single-cell statistical properties 45 during the transient. The bacterial reductive division is therefore an important model case for 46 studying cell size statistics under time-dependent environments and testing the robustness of the 47 scale invariance against environmental changes. 48 It has been, however, a challenge to observe large populations of bacteria under uniform yet 49 time-dependent growth conditions. For steady conditions, the Mother Machine (Wang et al. (2010)), 50 which allows for tracking of bacteria trapped in short narrow channels, was proved to be a powerful 51 tool for measuring cell size statistics. In such experiments, the channel width needs to be adapted 52 to cell widths in a given condition, and this renders the application to time-dependent conditions 53 difficult. If we enlarge the channels, depletion of nutrients in deeper regions of the channels 54 induces spatial heterogeneity, as discussed in ref.(Cho et al. (2007); Mather et al. (2010)) and later 55 in this article. Hence, it is als...

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“… 17 , our device could also provide a standardised tool for the in situ characterisation of the mechanical properties of biofilms. This is particularly relevant, given the recent acknowledgement of the absence of standardised methods to characterise the mechanical properties of biofilms 33 .…”

Section: Discussionmentioning

confidence: 99%

Magneto-mechanically actuated microstructures to efficiently prevent bacterial biofilm formation

Pichot¹,

Joisten²,

Grant³

et al. 2020

Sci Rep

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Biofilm colonisation of surfaces is of critical importance in various areas ranging from indwelling medical devices to industrial setups. Of particular importance is the reduced susceptibility of bacteria embedded in a biofilm to existing antimicrobial agents. In this paper, we demonstrate that remotely actuated magnetic cantilevers grafted on a substrate act efficiently in preventing bacterial biofilm formation. When exposed to an alternating magnetic field, the flexible magnetic cantilevers vertically deflect from their initial position periodically, with an extremely low frequency (0.16 Hz). The cantilevers’ beating prevents the initial stage of bacterial adhesion to the substrate surface and the subsequent biofilm growth. Our experimental data on E. coli liquid cultures demonstrate up to a 70% reduction in biofilm formation. A theoretical model has been developed to predict the amplitude of the cantilevers vertical deflection. Our results demonstrate proof-of-concept for a device that can magneto-mechanically prevent the first stage in bacterial biofilm formation, acting as on-demand fouling release active surfaces.

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Towards standardized mechanical characterization of microbial biofilms: analysis and critical review

Cited by 124 publications

References 132 publications

Nonlinear rheological characteristics of single species bacterial biofilms

Nonlinear rheological characteristics of single species bacterial biofilms

Scale invariance during bacterial reductive division observed by an extensive microperfusion system

Magneto-mechanically actuated microstructures to efficiently prevent bacterial biofilm formation

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