Exposure of Bacterial Biofilms to Electrical Current Leads to Cell Death Mediated in Part by Reactive Oxygen Species

Abstract

Bacterial biofilms may form on indwelling medical devices such as prosthetic joints, heart valves and catheters, causing challenging-to-treat infections. We have previously described the ‘electricidal effect’, in which bacterial biofilms are decreased following exposure to direct electrical current. Herein, we sought to determine if the decreased bacterial quantities are due to detachment of biofilms or cell death and to investigate the role that reactive oxygen species (ROS) play in the observed effect. Using confocal and electron microscopy and flow cytometry, we found that direct current (DC) leads to cell death and changes in the architecture of biofilms formed by Gram-positive and Gram-negative bacteria. Reactive oxygen species (ROS) appear to play a role in DC-associated cell death, as there was an increase in ROS-production by Staphylococcus aureus and Staphylococcus epidermidis biofilms following exposure to DC. An increase in the production of ROS response enzymes catalase and superoxide dismutase (SOD) was observed for S. aureus, S. epidermidis and Pseudomonas aeruginosa biofilms following exposure to DC. Additionally, biofilms were protected from cell death when supplemented with antioxidants and oxidant scavengers, including catalase, mannitol and Tempol. Knocking out SOD (sodAB) in P. aeruginosa led to an enhanced DC effect. Microarray analysis of P. aeruginosa PAO1 showed transcriptional changes in genes related to the stress response and cell death. In conclusion, the electricidal effect results in death of bacteria in biofilms, mediated, at least in part, by production of ROS.

Electroceutical Treatment of Pseudomonas aeruginosa Biofilms

“…A gold cathode with carbon and platinum anodes were reported to be the most effective against the urinary tract planktonic pathogens E. coli and P. mirabilis , while silver, nickel, or copper electrodes corroded to the point of breaking during experiments 17 . In another study, the authors showed application of direct current through platinum electrodes resulted in an increase in the production of reactive oxygen species (ROS) responsible for killing of S. aureus , S. epidermidis and P. aeruginosa biofilms 45 . It is certainly possible that other cidal agents besides HOCl may be active in the PA biofilm remediation observed in our results.…”

Biofilm dispersion: The key to biofilm eradication or opening Pandora’s box?

“…This bioelectric effect is not fully understood yet, although several factors potentially contributing to the increased efficacy have been described. The oxygen and reactive oxygen species (ROS) that are produced duringthe electrolysis of water contribute to the increased susceptibility [ 121 , 122 ]. In addition, the electric current reduces the antibiotic binding capabilities of the matrix and increases permeability of biofilm cells (electroporation), leading to an increased antibiotic uptake in the cells [ 122 ].…”

“…The oxygen and reactive oxygen species (ROS) that are produced duringthe electrolysis of water contribute to the increased susceptibility [ 121 , 122 ]. In addition, the electric current reduces the antibiotic binding capabilities of the matrix and increases permeability of biofilm cells (electroporation), leading to an increased antibiotic uptake in the cells [ 122 ]. The effect of a low electric current has also been evaluated in vivo using rabbits [ 123 ].…”

Demolishing the great wall of biofilms in Gram‐negative bacteria: To disrupt or disperse?

“…To effectively eradicate biofilms, many anti‐biofilm approaches have been developed, mainly mechanical removal of biofilms, which includes electricity and sonication, and chemotherapy, which is the focus of this review. Novel drug candidates must be developed for effective anti‐biofilm therapy of chronic infections in humans.…”