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Electrically induced bacterial membrane-potential dynamics correspond to cellular proliferation capacity
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Stratford, James P., Edwards, Conor L.A., Ghanshyam, Manjari J. , Malyshev, Dmitry, Delise, Marco A., Hayashi, Yoshikatsu and Asally, Munehiro (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 (9). pp. 9552-9557. doi:10.1073/pnas.1901788116 ISSN 0027-8424.
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Official URL: http://dx.doi.org/10.1073/pnas.1901788116
Abstract
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 microbiology. 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-second 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 membrane 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 antimicrobial agents at the single-cell level.
| Item Type: | Journal Article | ||||||||||||||||||
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| Subjects: | Q Science > QH Natural history | ||||||||||||||||||
| Divisions: | Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- ) | ||||||||||||||||||
| Library of Congress Subject Headings (LCSH): | Cell membranes -- Electric properties, Electrophysiology | ||||||||||||||||||
| Journal or Publication Title: | Proceedings of the National Academy of Sciences of the United States of America | ||||||||||||||||||
| Publisher: | National Academy of Sciences | ||||||||||||||||||
| ISSN: | 0027-8424 | ||||||||||||||||||
| Official Date: | May 2019 | ||||||||||||||||||
| Dates: |
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| Volume: | 116 | ||||||||||||||||||
| Number: | 9 | ||||||||||||||||||
| Page Range: | pp. 9552-9557 | ||||||||||||||||||
| DOI: | 10.1073/pnas.1901788116 | ||||||||||||||||||
| Status: | Peer Reviewed | ||||||||||||||||||
| Publication Status: | Published | ||||||||||||||||||
| Access rights to Published version: | Open Access (Creative Commons) | ||||||||||||||||||
| Date of first compliant deposit: | 24 April 2019 | ||||||||||||||||||
| Date of first compliant Open Access: | 25 April 2019 | ||||||||||||||||||
| RIOXX Funder/Project Grant: |
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