Viscoelastic response of<i>Escherichia coli</i>biofilms to genetically altered expression of extracellular matrix components

Horvat, Maruša; Pannuri, Archana; Romeo, Tony; Dogša, Iztok; Stopar, David

doi:10.1039/c9sm00297a

Cited by 29 publications

(34 citation statements)

References 63 publications

(72 reference statements)

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“…While the potential of glycoside hydrolases and DNase I as biofilm dispersal agents has been previously described in the literature (19,22), the originality of our work resides in the association of enzymes targeting biofilm matrix components found in biofilms of varied species (28), which is hypothesized to help sidestep the limited spectrum of individual enzymes caused by the significant variations in matrix contents observed among bacterial species and strains (29,30). Indeed, the results of individual enzymes assays performed in this study underline the added value of combining enzymes as done in the TEC.…”

Section: Discussionmentioning

confidence: 99%

“…The β-1,6hexosaminidase used in this study is a Dispersin B homolog targeting the poly-β-1,6-Nacetylglucosamine (PNAG) component of the biofilm matrix (31,32). PNAG is an important constituent of the matrix of multiple species' biofilms and is required for the formation of biofilm by S. epidermidis (30,33,34) and S. aureus strains expressing the icaABCD operon (30,35) and of E. coli strains expressing the pgaABCD locus (29,36). Dispersin B was shown to disperse the biofilms of PNAG-producing strains of multiple species, including those included in our study (20,37,38).…”

Section: Discussionmentioning

confidence: 99%

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In VitroStudy of the Synergistic Effect of an Enzyme Cocktail and Antibiotics against Biofilms in a Prosthetic Joint Infection Model

Poilvache

Ruiz-Sorribas

Bambeke

2021

Antimicrob Agents Chemother

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Prosthetic Joint Infections (PJI) are frequent complications of arthroplasties. Their treatment is made complex by the rapid formation of bacterial biofilms, limiting the effectiveness of antibiotic therapy. In this study, we explore the effect of a tri-enzymatic cocktail (TEC) consisting of an endo-1,4-β-d-glucanase, a β-1,6-hexosaminidase, and an RNA/DNA nonspecific endonuclease combined with antibiotics of different classes against biofilms of S. aureus, S. epidermidis, and E. coli grown on Ti6Al4V substrates. Biofilms were grown in TSB with 10g/L glucose and 20g/L NaCl (TGN). Mature biofilms were assigned to a control group or treated with the TEC for 30 min, then either analyzed or reincubated for 24h in TGN or TGN with antibiotics. The cytotoxicity of the TEC was assayed against MG-63 osteoblasts, primary murine fibroblasts, and J-774 macrophages using the LDH release test. The TEC dispersed 80.3 to 95.2% of the biofilms’ biomass after 30 min. The reincubation of the treated biofilms with antibiotics resulted in a synergistic reduction of the total culturable bacterial count (CFU) compared to biofilms treated with antibiotics alone in the three tested species (additional reduction from 2 to more than 3 log10 CFU). No toxicity of the TEC was observed against the tested cell lines after a 24 h of incubation. The combination of pretreatment with TEC followed by a 24 h of incubation with antibiotics had a synergistic effect against biofilms of S. aureus, S. epidermidis, and E. coli. Further studies should assess the potential of the TEC as an adjuvant therapy in in vivo models of PJI.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

In VitroStudy of the Synergistic Effect of an Enzyme Cocktail and Antibiotics against Biofilms in a Prosthetic Joint Infection Model

Poilvache

Ruiz-Sorribas

Bambeke

2021

Antimicrob Agents Chemother

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“…The elongational viscosity of a streamer is also proportional to the damping coefficient of cell–cell adhesion force and the spring constant has no significant influence on its value. The non-dimensional viscosity

is up to 600, which can be estimated as μ s is up to 0.6 Pa s. This value is much smaller than the typical viscosity of bacterial biofilms: 10 3 to 10 5 Pa s [ 2 , 4 , 18 , 20 ]. Accordingly, the relaxation time in the present study is much smaller than the experimental results: 0.01 s versus 10 3 s, respectively.…”

Section: Resultsmentioning

confidence: 96%

“…A number of studies on the rheological properties of biofilms using several measurement techniques, including rheometry, uniaxial compression, atomic force microscopy and hydrodynamic load, indicated that biofilms are viscoelastic [4,[17][18][19][20][21]. The elastic modulus and viscosity of biofilms vary widely between cell types and growth stages, with shear modulus ranging from 10 −2 to 10 6 Pa [1].…”

Section: Introductionmentioning

confidence: 99%

Impact of rheological properties on bacterial streamer formation

Kitamura

Omori

Ishikawa

2021

J. R. Soc. Interface.

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Bacterial biofilms, which can be found wherever there is water and a substrate, can cause chronic infections and clogging of industrial flow systems. Despite intensive investigation of the dynamics and rheological properties of biofilms, the impact of their rheological properties on streamer growth remains unknown. We numerically simulated biofilm growth in a pillar-flow and investigated the effects of rheological properties of a filamentous flow-shaped biofilm, called a ‘streamer’, on its formation by varying the viscoelasticity. The flow-field is assumed to be a Stokes flow and is solved by a boundary element method. A Maxwell model is used for extracellular matrix-mediated streamer growth to express the fluidity of streamer formations. Both high elastic modulus and viscosity are needed for streamer formation, and high viscosity promotes streamer growth at low cell concentrations. Our findings are consistent with experimental observations and can explain the relationship between the cell concentrations and viscosity at which streamers form.

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“…Curli deficient E. coli mutants (UTI89 ∆ csgA , UTI89 ∆ bcsG ∆ csgA , UTI89 ∆ bcsA ∆ csgA , AR3110 ∆ csgBA , AR3110 ∆ bcsG ∆ csgBA , and AR3110 ∆ bcsA ∆ csgBA) exhibit severely reduced CV retention and do not adhere well to plastic (Figure 6), in agreement with previous work in some strains, including UTI89. [ 53,64,82,89–91 ] Thus, to the extent to which plastic associated biofilm is evaluated in a standard biomass accumulation assay for cells grown in YESCA broth, biofilm formation is dominated by curli production in UTI89 and AR3110.…”

Section: Resultsmentioning

confidence: 99%

Variation in the ratio of curli and phosphoethanolamine cellulose associated with biofilm architecture and properties

et al. 2020

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Bacterial biofilms are communities of bacteria entangled in a self‐produced extracellular matrix (ECM). Escherichia coli direct the assembly of two insoluble biopolymers, curli amyloid fibers, and phosphoethanolamine (pEtN) cellulose, to build remarkable biofilm architectures. Intense curiosity surrounds how bacteria harness these amyloid‐polysaccharide composites to build biofilms, and how these biopolymers function to benefit bacterial communities. Defining ECM composition involving insoluble polymeric assemblies poses unique challenges to analysis and, thus, to comparing strains with quantitative ECM molecular correlates. In this work, we present results from a sum‐of‐the‐parts 13C solid‐state nuclear magnetic resonance (NMR) analysis to define the curli‐to‐pEtN cellulose ratio in the isolated ECM of the E. coli laboratory K12 strain, AR3110. We compare and contrast the compositional analysis and comprehensive biofilm phenotypes for AR3110 and a well‐studied clinical isolate, UTI89. The ECM isolated from AR3110 contains approximately twice the amount of pEtN cellulose relative to curli content as UTI89, revealing plasticity in matrix assembly principles among strains. The two parent strains and a panel of relevant gene mutants were investigated in three biofilm models, examining: (a) macrocolonies on agar, (b) pellicles at the liquid‐air interface, and (c) biomass accumulation on plastic. We describe the influence of curli, cellulose, and the pEtN modification on biofilm phenotypes with power in the direct comparison of these strains. The results suggest that curli more strongly influence adhesion, while pEtN cellulose drives cohesion. Their individual and combined influence depends on both the biofilm modality (agar, pellicle, or plastic‐associated) and the strain itself.

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Viscoelastic response ofEscherichia colibiofilms to genetically altered expression of extracellular matrix components

Abstract: How the viscoelastic properties of the extracellular matrix affect the various biological functions conferred by biofilms is an important question in microbiology.

Cited by 29 publications

References 63 publications

In VitroStudy of the Synergistic Effect of an Enzyme Cocktail and Antibiotics against Biofilms in a Prosthetic Joint Infection Model

In VitroStudy of the Synergistic Effect of an Enzyme Cocktail and Antibiotics against Biofilms in a Prosthetic Joint Infection Model

Impact of rheological properties on bacterial streamer formation

Variation in the ratio of curli and phosphoethanolamine cellulose associated with biofilm architecture and properties

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