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Anomalous diffusion of nanoparticles in the spatially heterogeneous biofilm environment.

ABSTRACT: Biofilms contain extracellular polymeric substances (EPS) that provide structural support and restrict penetration of antimicrobial treatment. To overcome limited penetration, functionalized nanoparticles (NPs) have been suggested as carriers for antimicrobial delivery. Using microscopy, we evaluate the diffusion of nanoparticles in function of the structure of Salmonella biofilms. We observe anomalous diffusion and heterogeneous mobility of NPs resulting in distinct NPs distribution that depended on biofilm structure. Through Brownian dynamics modeling with spatially varying viscosity around bacteria, we demonstrated that spatial gradients in diffusivity generate viscous sinks that trap NPs near bacteria. This model replicates the characteristic diffusion signature and vertical distribution of NPs in the biofilm. From a treatment perspective, our work indicates that both biofilm structure and the level of EPS can impact NP drug delivery, where low levels of EPS might benefit delivery by immobilizing NPs closer to bacteria and higher levels hamper delivery due to shielding effects.

SUBMITTER: Coppens B

PROVIDER: S-EPMC10227381 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Anomalous diffusion of nanoparticles in the spatially heterogeneous biofilm environment.

Coppens Bart B Belpaire Tom E R TER Pešek Jiří J Steenackers Hans P HP Ramon Herman H Smeets Bart B

iScience 20230513 6

Biofilms contain extracellular polymeric substances (EPS) that provide structural support and restrict penetration of antimicrobial treatment. To overcome limited penetration, functionalized nanoparticles (NPs) have been suggested as carriers for antimicrobial delivery. Using microscopy, we evaluate the diffusion of nanoparticles in function of the structure of Salmonella biofilms. We observe anomalous diffusion and heterogeneous mobility of NPs resulting in distinct NPs distribution that depend ...[more]

PMID: 37260744

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Project description:Biofilms are abundantly present in both natural and engineered environmental systems and will likely influence broader particle fate and transport phenomena. While some developed models describe the interactions between nanoparticles and biofilms, studies are only beginning to uncover the complexity of nanoparticle diffusion patterns. With the knowledge of the nanoparticle potential to influence bacterial processes, more systematic studies are needed to uncover the dynamics of bacteria-nanoparticle interactions. This study explored specific microbial responses to nanoparticles and the heterogeneity of nanoparticle diffusion. Pseudomonas aeruginosa biofilms (cultivated for 48 and 96 hours, representing early and late stages of development) were exposed to charged (aminated and carboxylated) polystyrene nanoparticles. With a combination of advanced fluorescence microscopy and real time quantitative PCR, we characterized the diffusion of polystyrene nanoparticles in P. aeruginosa biofilms and evaluated how biofilms respond to the presence of nanoparticles in terms of the expression of key EPS production-associated genes (pelA and rpsL) and quorum-sensing associated (lasR) genes. Our findings show that nanoparticle diffusion coefficients are independent of the particle surface charge only in mature biofilms and that the presence of nanoparticles influences bacterial gene expression. Independent of the particle's charge polystyrene nanoparticles down-regulated pelA in mature biofilms. By contrast, charge-specific responses were identified in lasR and rpsL gene expression. The targeted genes expression analysis and heterogeneous diffusion models demonstrate that particle charge influences nanoparticle mobility and provides significant insight into the intrinsic structural heterogeneity of P. aeruginosa biofilms. These findings suggest that biofilm maturity and particle charge are essential factors to consider when evaluating the transport of nanoparticles within a biofilm matrix.

Dataset Information

Anomalous diffusion of nanoparticles in the spatially heterogeneous biofilm environment.

Publications

Anomalous diffusion of nanoparticles in the spatially heterogeneous biofilm environment.

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