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Escherichia coli’s physiology can turn membrane voltage dyes into actuators

L Mancini, G Terradot, T Tian, Y Pu, Y Li, View ORCID ProfileCJ Lo, F Bai, T Pilizota
doi: https://doi.org/10.1101/607838
L Mancini
1Centre for Synthetic and Systems Biology
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G Terradot
1Centre for Synthetic and Systems Biology
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T Tian
2BIOPIC, School of Life Sciences, Peking University
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Y Pu
2BIOPIC, School of Life Sciences, Peking University
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Y Li
2BIOPIC, School of Life Sciences, Peking University
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CJ Lo
3Biodynamic Optical Imaging Center, Peking University
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  • ORCID record for CJ Lo
F Bai
2BIOPIC, School of Life Sciences, Peking University
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T Pilizota
1Centre for Synthetic and Systems Biology
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  • For correspondence: teuta.pilizota@ed.ac.uk
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ABSTRACT

The electrical membrane potential (Vm) is one of the components of the electrochemical potential of protons across the biological membrane (proton motive force), which powers many vital cellular processes, and Vm also plays a role in signal transduction. Therefore, measuring it is of great interest, and over the years a variety of techniques has been developed for the purpose. In bacteria, given their small size, Nernstian membrane voltage probes are arguably the favourite strategy, and their cytoplasmic accumulation depends on Vm according to the Nernst equation. However, a careful calibration of Nernstian probes that takes into account the trade-offs between the ease with which the signal from the dye is observed, and the dyes’ interactions with cellular physiology, is rarely performed. Here we use a mathematical model to understand such trade-offs and, based on the knowledge gained, propose a general work-flow for the characterization of Nernstian dye candidates. We demonstrate the work-flow on the Thioflavin T dye in Escherichia coli, and identify conditions in which the dye turns from a Vm probe into an actuator.

SIGNIFICANCE STATEMENT

The phospholipid bilayer of a biological membrane is virtually impermeable to charged molecules. Much like in a rechargeable battery, cells harness this property to store an electrical potential that fuels life reactions but also transduces signals. Measuring this electrical potential, also referred to as membrane voltage, is therefore of great interest and a variety of techniques have been employed for the purpose, starting as early as the 1930s. For the case of bacteria, which are smaller in size and possess a stiffer cell wall, arguably the most popular approach to measuring membrane voltage are Nernstian probes that accumulate across the bacterial membrane according to the Nernst potential. The present study characterizes the undesired effects Nernstian probes can have on cell physiology, which can be crucial for the accurate interpretation of experimental results. Using mathematical modelling and experiments, the study provides a general, simple workflow to characterise and minimise these effects.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted April 12, 2019.
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Escherichia coli’s physiology can turn membrane voltage dyes into actuators
L Mancini, G Terradot, T Tian, Y Pu, Y Li, CJ Lo, F Bai, T Pilizota
bioRxiv 607838; doi: https://doi.org/10.1101/607838
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Escherichia coli’s physiology can turn membrane voltage dyes into actuators
L Mancini, G Terradot, T Tian, Y Pu, Y Li, CJ Lo, F Bai, T Pilizota
bioRxiv 607838; doi: https://doi.org/10.1101/607838

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