Electrical Signalling and the Neuronal-like Behaviour of Escherichia coli Biofilms

Abstract

Bacteria biofilms are communities of microorganisms that attach to surfaces. They cause infections and have a significant impact on the environment. Ion channel-mediated electrical signalling has not been previously studied in Escherichia coli biofilms. Fluorescence microscopy and electrochemical impedance spectroscopy were used to study electrical signalling and the neuronal-like behaviour of Escherichia coli biofilms, respectively. Escherichia coli biofilms engage in community-level synchronized membrane potential dynamics when subjected to 440 nm antimicrobial blue light stress. Two hyperpolarization events were observed in response to light stress. The first peak is when Escherichia coli first registers the presence of an external stressor in their vicinity, which is mediated by the mechanically sensitive ion channels (MscK, MscL and MscS). The depolarization and subsequent second peak that occurs in response to continued stimulation corresponds to a habituation phenomenon and is mediated by the Escherichia coli potassium channel, the Kch. The biophysical mechanisms of the electrical signalling were probed using the Hodgkin-Huxley model. The electrical signalling phenomena were also characterized using a 3D fire-diffuse-fire agent-based model. The model revealed that long-range electrical signalling in Escherichia coli biofilms involved potassium ions and the propagating wavefront exhibits different properties for both the centripetal and centrifugal travel. Escherichia coli biofilms exhibit significant stable negative capacitances at low frequencies when they experience a small bias voltage in electrical impedance spectroscopy experiments. The frequency domain Hodgkin-Huxley model and equivalent electric circuit were used to establish the frequency response of Escherichia coli biofilms to the small amplitude voltage perturbations and characterize the conditions for the emergence of this neuronal-like effect in biofilms. The importance of the voltage-gated potassium channel, Kch, in the negative capacitance was demonstrated using knock-down mutants. Overall, this study reveals a novel electrical signalling phenomenon in Escherichia coli biofilms and the unique role of the Kch potassium ion channel in the electrical signalling. The work provides a new outlook on the emergent electrophysiology of bacterial biofilms.

Date of Award	1 Aug 2024
Original language	English
Awarding Institution	The University of Manchester
Supervisor	Ian Roberts (Supervisor) & Thomas Waigh (Supervisor)