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Electrically induced bacterial membrane-potential dynamics correspond to cellular proliferation capacity

Stratford, J. P., Edwards, C. L. A., Ghanshyam, M. J., Malyshev, D., Delise, M. A., Hayashi, Y. ORCID: https://orcid.org/0000-0002-9207-6322 and Asally, M. (2019) Electrically induced bacterial membrane-potential dynamics correspond to cellular proliferation capacity. Proceedings of the National Academy of Sciences of the United States of America, 116 (19). pp. 9552-9557. ISSN 1091-6490

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To link to this item DOI: 10.1073/pnas.1901788116

Abstract/Summary

Membrane-potential dynamics mediate bacterial electrical signaling at both intra- and intercellular levels. Membrane potential is also central to cellular proliferation. It is unclear whether the cellular response to external electrical stimuli is influenced by the cellular proliferative capacity. A new strategy enabling electrical stimulation of bacteria with simultaneous monitoring of single-cell membrane- potential dynamics would allow bridging this knowledge gap and further extend electrophysiological studies into the field of microbi- ology. Here we report that an identical electrical stimulus can cause opposite polarization dynamics depending on cellular proliferation capacity. This was demonstrated using two model organisms, namely Bacillus subtilis and Escherichia coli, and by developing an apparatus enabling exogenous electrical stimulation and single-cell time-lapse microscopy. Using this bespoke apparatus, we show that a 2.5-sec- ond electrical stimulation causes hyperpolarization in unperturbed cells. Measurements of intracellular K+ and the deletion of the K+ channel suggested that the hyperpolarization response is caused by the K+ efflux through the channel. When cells are preexposed to 400 ± 8 nm wavelength light, the same electrical stimulation depolarizes cells instead of causing hyperpolarization. A mathematical model extended from the FitzHugh–Nagumo neuron model suggested that the opposite response dynamics are due to the shift in resting mem- brane potential. As predicted by the model, electrical stimulation only induced depolarization when cells are treated with antibiotics, protonophore, or alcohol. Therefore, electrically induced membrane- potential dynamics offer a reliable approach for rapid detection of proliferative bacteria and determination of their sensitivity to anti- microbial agents at the single-cell level.

Item Type:Article
Refereed:Yes
Divisions:Life Sciences > School of Biological Sciences > Department of Bio-Engineering
ID Code:83508
Publisher:National Academy of Sciences

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