Spatial propagation of electrical signals in circular biofilms: A combined experimental and agent-based fire-diffuse-fire study

Abstract

Bacterial biofilms are a risk to human health, playing critical roles in persistent infections. Recent studies have observed electrical signaling in biofilms and thus biofilms represent a new class of active excitable matter in which cell division is the active process and the spiking of the individual bacterial cells is the excitable process. Electrophysiological models have predominantly been developed to describe eukaryotic systems, but we demonstrate their use in understanding bacterial biofilms. Our agent-based fire-diffuse-fire (ABFDF) model successfully simulates the propagation of both centrifugal (away from the center) and centripetal (toward the center) electrical signals through biofilms of Bacillus subtilis. Furthermore, the ABFDF model allows realistic spatial positioning of the bacteria in two dimensions to be included in the fire-diffuse-fire model and this is the crucial factor that improves agreement with experiments. The speed of propagation is not constant and depends on the radius of the propagating electrical wave front. Centripetal waves are observed to move faster than centrifugal waves, which is a curvature driven effect and is correctly captured by our simulations.

Emergence of ion-channel mediated electrical oscillations inEscherichia colibiofilms

“…Furthermore, the results confirm that curvature affects the motion of the wavefronts 38 . Blee and co-workers 5 previously observed a superdiffusive wave motion for both the centrifugal (𝛾 = 1.42 ± 0.06ሻ and centripetal phases (𝛾 = 1.79 ± 0.03ሻ of the potassium wave in 2D B. subtilis biofilm. The centripetal waves appear to travel faster than the centrifugal wave.…”

“…It enables communication in bacterial biofilms due to the transmission of potassium wavefronts in the local environment of the biofilm. The potassium wavefront occurs in both centripetal and centrifugal varieties 5 and emerges spontaneously after the biofilm has grown to a critical size 6 . Photodynamic therapy using blue light causes a process of stage-dependent cell dispersal in biofilms and membrane hyperpolarization 7 .…”

Heterogeneous anomalous transport in cellular and molecular biology

“…• Numerous new physical phenomena are still left to be discovered that are related to heterogeneous anomalous transport e.g. the motility of molecular motors in active matter [104], collective cellular motility in embryos [74], the motion of wavefronts of electrical signalling in bacterial biofilms [50] and how bacteria swim [333]. The field provides an interesting perspective to the subject of soft matter physics, focusing on the statistics of motility.…”

“…Heterogeneity due to the curvature of substrates, varying diffusion coefficients, varying local geometry (porous materials and gels) and varying density will all affect the propagation of the RD wavefronts. A specific example is electrical signalling in bacterial biofilms [50] e.g. the speed of propagation of wavefronts of potassium ions in a mushroom-shaped biofilm will be affected by the local curvature of the mushrooms.…”

Electrical Impedance Spectroscopy with Bacterial Biofilms: Neuronal-like Behavior

“…9,22 Bacteria in biofilms can have membrane potential spiking similar to neurons, 23−30 although the hyperpolarization phenomena tend to be more varied than the stereotyped spiking events observed in neuronal cells. In the presence of external stimuli, such as metabolic stress, 24 photooxidative stress, 25,30 biosurfactants, 31 and external electrical stress, 32 cells in biofilms open their voltage-gated channels to allow the flow of cationic ions. In Bacillus subtilis (B. subtilis) biofilms, the YugO channel controls the flux of potassium ions and is implicated in electrical signaling.…”