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Abstract

Bacterial ion fluxes are involved in the generation of energy, transport, and motility. As such, bacterial electrophysiology is fundamentally important for the bacterial life cycle, but it is often neglected and consequently, by and large, not understood. Arguably, the two main reasons for this are the complexity of measuring relevant variables in small cells with a cell envelope that contains the cell wall and the fact that, in a unicellular organism, relevant variables become intertwined in a nontrivial manner. To help give bacterial electrophysiology studies a firm footing, in this review, we go back to basics. We look first at the biophysics of bacterial membrane potential, and then at the approaches and models developed mostly for the study of neurons and eukaryotic mitochondria. We discuss their applicability to bacterial cells. Finally, we connect bacterial membrane potential with other relevant (electro)physiological variables and summarize methods that can be used to both measure and influence bacterial electrophysiology.

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2024-07-16
2024-10-10
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Literature Cited

  1. 1.
    Ackerman JJH, Soto GE, Spees WM, Zhu Z, Evelhoch JL. 1996.. The NMR chemical shift pH measurement revisited: analysis of error and modeling of a pH dependent reference. . Magn. Reson. Med. 36::64783
    [Crossref] [Google Scholar]
  2. 2.
    Agmon N, Gutman M. 2011.. Bioenergetics: proton fronts on membranes. . Nat. Chem. 3:(11):84042
    [Crossref] [Google Scholar]
  3. 3.
    Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. 2004.. Molecular Biology of the Cell. New York:: Garland Sci.
    [Google Scholar]
  4. 4.
    Amorino GP, Fox MH. 1995.. Intracellular Na+ measurements using sodium green tetraacetate with flow cytometry. . Cytometry 21::24856
    [Crossref] [Google Scholar]
  5. 5.
    Apell H-J. 2004.. How do P-type ATPases transport ions?. Bioelectrochemistry 63::14956
    [Crossref] [Google Scholar]
  6. 6.
    Arlt J, Martinez VA, Dawson A, Pilizota T, Poon WCK. 2018.. Painting with light-powered bacteria. . Nat. Commun. 9::768
    [Crossref] [Google Scholar]
  7. 7.
    Arnold WM, Zimmermann U. 1982.. Rotating-field-induced rotation and measurement of the membrane capacitance of single mesophyll cells of Avena sativa. . Z. Naturforsch. 37::90815
    [Crossref] [Google Scholar]
  8. 8.
    Asai Y, Yakushi T, Kawagishi I, Homma M. 2003.. Ion-coupling determinants of Na+-driven and H+-driven flagellar motors. . J. Mol. Biol. 327::45363
    [Crossref] [Google Scholar]
  9. 9.
    Atkins P, De Paula J. 2006.. Atkins' Physical Chemistry. New York:: W.H. Freeman
    [Google Scholar]
  10. 10.
    Bazant MZ, Kilic MS, Storey BD, Ajdari A. 2009.. Towards an understanding of induced-charge electrokinetics at large applied voltages in concentrated solutions. . Adv. Colloid Interface Sci. 152::4888
    [Crossref] [Google Scholar]
  11. 11.
    Beard DA. 2005.. A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation. . PLOS Comput. Biol. 1:(4):e36. Erratum. 2006.. PLOS Comput. Biol. 2:(1):e8
    [Google Scholar]
  12. 12.
    Beard DA, Qian H. 2007.. Relationship between thermodynamic driving force and one-way fluxes in reversible processes. . PLOS ONE 2:(1):e144
    [Crossref] [Google Scholar]
  13. 13.
    Beard DA, Qian H. 2008.. Chemical Biophysics: Quantitative Analysis of Cellular Systems. Cambridge, UK:: Cambridge Univ. Press
    [Google Scholar]
  14. 14.
    Bearne SL. 2014.. Illustrating the effect of pH on enzyme activity using Gibbs energy profiles. . J. Chem. Educ. 91::8490
    [Crossref] [Google Scholar]
  15. 15.
    Berg HC. 2003.. The rotary motor of bacterial flagella. . Annu. Rev. Biochem. 72::1954
    [Crossref] [Google Scholar]
  16. 16.
    Berry RM, Berg HC. 1997.. Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers. . PNAS 94::1443337
    [Crossref] [Google Scholar]
  17. 17.
    Biquet-Bisquert A, Carrio B, Meyer N, Fernandes TFD, Abkarian M, et al. 2023.. Spatio-temporal dynamics of the proton motive force on single bacterial cells. . bioRxiv 2023.04.03.535353. https://doi.org/10.1101/2023.04.03.535353
  18. 18.
    Biquet-Bisquert A, Labesse G, Pedaci F, Nord AL. 2021.. The dynamic ion motive force powering the bacterial flagellar motor. . Front. Microbiol. 12::659464
    [Crossref] [Google Scholar]
  19. 19.
    Booth IR, Higgins CF. 1990.. Enteric bacteria and osmotic stress: intracellular potassium glutamate as a secondary signal of osmotic stress?. FEMS Microbiol. Rev. 75::23946
    [Crossref] [Google Scholar]
  20. 20.
    Bot CT, Prodan C. 2010.. Quantifying the membrane potential during E. coli growth stages. . Biophys. Chem. 146::13337
    [Crossref] [Google Scholar]
  21. 21.
    Bruni GN, Weekley RA, Dodd BJT, Kralj JM. 2017.. Voltage-gated calcium flux mediates Escherichia coli mechanosensation. . PNAS 114::944550
    [Crossref] [Google Scholar]
  22. 22.
    Buttress JA, Halte M, Te Winkel JD, Erhardt M, Popp PF, Strahl H. 2022.. A guide for membrane potential measurements in Gram-negative bacteria using voltage-sensitive dyes. . Microbiology 168::001227
    [Crossref] [Google Scholar]
  23. 23.
    Caldwell PC. 1956.. Intracellular pH. . Int. Rev. Cytol. 5::22977
    [Crossref] [Google Scholar]
  24. 24.
    Campbell DT, Hille B. 1976.. Kinetic and pharmacological properties of the sodium channel of frog skeletal muscle. . J. Gen. Physiol. 67::30923
    [Crossref] [Google Scholar]
  25. 25.
    Castle AM, Macnab RM, Shulman RG. 1986.. Measurement of intracellular sodium concentration and sodium transport in Escherichia coli by 23Na nuclear magnetic resonance. . J. Biol. Chem. 261::328894
    [Crossref] [Google Scholar]
  26. 26.
    Chakraborty S, Mizusaki H, Kenney LJ. 2015.. A FRET-based DNA biosensor tracks OmpR-dependent acidification of Salmonella during macrophage infection. . PLOS Biol. 13::e1002116
    [Crossref] [Google Scholar]
  27. 27.
    Chakraborty S, Winardhi RS, Morgan LK, Yan J, Kenney LJ. 2017.. Non-canonical activation of OmpR drives acid and osmotic stress responses in single bacterial cells. . Nat. Commun. 8::1587
    [Crossref] [Google Scholar]
  28. 28.
    Chapman DL. 1913.. A contribution to the theory of electrocapillarity. . Lond. Edinb. Dublin Philos. Mag. J. Sci. 25::47581
    [Crossref] [Google Scholar]
  29. 29.
    Chimerel C, Field CM, Piñero-Fernandez S, Keyser UF, Summers DK. 2012.. Indole prevents Escherichia coli cell division by modulating membrane potential. . Biochim. Biophys. Acta Biomembr. 1818::159094
    [Crossref] [Google Scholar]
  30. 30.
    Cremer J, Honda T, Tang Y, Wong-Ng J, Vergassola M, Hwa T. 2019.. Chemotaxis as a navigation strategy to boost range expansion. . Nature 575::65863
    [Crossref] [Google Scholar]
  31. 31.
    De Souza-Guerreiro TC, Bondelli G, Grobas I, Donini S, Sesti V, et al. 2023.. Membrane targeted azobenzene drives optical modulation of bacterial membrane potential. . Adv. Sci. 10::2205007
    [Crossref] [Google Scholar]
  32. 32.
    Debye P, Hückel E. 1923.. Zur Theorie der Elektrolyte. I. Gefrierpunktserniedrigung und verwandte Erscheinungen. . Phys. Z. 24::185206
    [Google Scholar]
  33. 33.
    Demchenko AP, Yesylevskyy SO. 2009.. Nanoscopic description of biomembrane electrostatics: results of molecular dynamics simulations and fluorescence probing. . Chem. Phys. Lipids 160::6384
    [Crossref] [Google Scholar]
  34. 34.
    Dibrova DV, Galperin MY, Koonin EV, Mulkidjanian AY. 2015.. Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics. . Biochemistry 80::495516
    [Google Scholar]
  35. 35.
    Dodge FA, Frankenhaeuser B. 1958.. Membrane currents in isolated frog nerve fibre under voltage clamp conditions. . J. Physiol. 143::7690
    [Crossref] [Google Scholar]
  36. 36.
    Dodge FA, Frankenhaeuser B. 1959.. Soidum currents in the myelinated nerve fibre of Xenopus laevis investigated with the voltage clamp technique. . J. Physiol. 148::188200
    [Crossref] [Google Scholar]
  37. 37.
    Dominguez DC. 2004.. Calcium signalling in bacteria. . Mol. Microbiol. 54::29197
    [Crossref] [Google Scholar]
  38. 38.
    Donnan FG. 1911.. Theorie der Membrangleichgewichte und Membranpotentiale bei Vorhandensein von nicht dialysierenden Elektrolyten. Ein Beitrag zur physikalisch-chemischen Physiologie. . Z. Elektrochem. Angew. Phys. Chem. 17::57281
    [Google Scholar]
  39. 39.
    Epstein W. 1986.. Osmoregulation by potassium transport in Escherichia coli. . FEMS Microbiol. Rev. 39::7378
    [Crossref] [Google Scholar]
  40. 40.
    Epstein W. 2003.. The roles and regulation of potassium in bacteria. . Prog. Nucleic Acid Res. Mol. Biol. 75::293320
    [Crossref] [Google Scholar]
  41. 41.
    Epstein W, Schultz SG. 1965.. Cation transport in Escherichia coli. . J. Gen. Physiol. 49::22134
    [Crossref] [Google Scholar]
  42. 42.
    Eyring H, Eyring EM. 1963.. Modern Chemical Kinetics. New York:: Reinhold
    [Google Scholar]
  43. 43.
    Felle H, Porter JS, Slayman CL, Kaback HR. 1980.. Quantitative measurements of membrane potential in Escherichia coli. . Biochemistry 19::358590
    [Crossref] [Google Scholar]
  44. 44.
    Feynman RP, Leighton RB, Sands M. 2011.. The Feynman Lectures on Physics. New York:: Basic Books
    [Google Scholar]
  45. 45.
    Francia S, Shmal D, Di Marco S, Chiaravalli G, Maya-Vetencourt JF, et al. 2022.. Light-induced charge generation in polymeric nanoparticles restores vision in advanced-stage retinitis pigmentosa rats. . Nat. Commun. 13::3677
    [Crossref] [Google Scholar]
  46. 46.
    Frankenhaeuser B. 1960.. Quantitative description of sodium currents in myelinated nerve fibres of Xenopus laevis. . J. Physiol. 151::491501
    [Crossref] [Google Scholar]
  47. 47.
    Frankenhaeuser B. 1960.. Sodium permeability in toad nerve and in squid nerve. . J. Physiol. 152::15966
    [Crossref] [Google Scholar]
  48. 48.
    Frankenhaeuser B. 1963.. A quantitative description of potassium currents in myelinated nerve fibres of Xenopus laevis. . J. Physiol. 169::42430
    [Crossref] [Google Scholar]
  49. 49.
    Fricke H. 1923.. The electric capacity of cell suspension. . Phys. Rev. 21::7089
    [Google Scholar]
  50. 50.
    Froschauer EM, Kolisek M, Dieterich F, Schweigel M, Schweyen RJ. 2004.. Fluorescence measurements of free [Mg2+] by use of mag-fura 2 in Salmonella enterica. . FEMS Microbiol. Lett. 237::4955
    [Google Scholar]
  51. 51.
    Fung DC, Berg HC. 1995.. Powering the flagellar motor of Escherichia coli with an external voltage source. . Nature 375::80912
    [Crossref] [Google Scholar]
  52. 52.
    Furst AL, Francis MB. 2019.. Impedance-based detection of bacteria. . Chem. Rev. 119::70026
    [Crossref] [Google Scholar]
  53. 53.
    Gabel CV, Berg HC. 2003.. The speed of the flagellar rotary motor of Escherichia coli varies linearly with protonmotive force. . PNAS 100::874851
    [Crossref] [Google Scholar]
  54. 54.
    Gabrielyan L, Sargsyan H, Trchounian A. 2015.. Novel properties of photofermentative biohydrogen production by purple bacteria Rhodobacter sphaeroides: effects of protonophores and inhibitors of responsible enzymes. . Microb. Cell Fact. 14::131
    [Crossref] [Google Scholar]
  55. 55.
    Galvani L. 1791.. De viribus electricitatis in motu musculari commentarius. . Bononiensi Sci. Artium Inst. Atque Acad. Comment. 7::363418
    [Google Scholar]
  56. 56.
    Gangola P, Rosen BP. 1987.. Maintenance of intracellular calcium in Escherichia coli. . J. Biol. Chem. 262::1257074
    [Crossref] [Google Scholar]
  57. 57.
    Garlid KD, Beavis AD, Ratkje SK. 1989.. On the nature of ion leaks in energy-transducing membranes. . Biochim. Biophys. Acta Bioenerg. 976::10920
    [Crossref] [Google Scholar]
  58. 58.
    Gasser B, Saloheimo M, Rinas U, Dragosits M, Rodríguez-Carmona E, et al. 2008.. Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. . Microb. Cell Fact. 7::11
    [Crossref] [Google Scholar]
  59. 59.
    Gheorghiu E. 2011.. Relating membrane potential to impedance spectroscopy. . J. Electr. Bioimpedance 2::9397
    [Crossref] [Google Scholar]
  60. 60.
    Gibbs GW. 1928.. The Collected Works of J. Willard Gibbs, Vol. I: Thermodynamics, ed. WR Longley, RG van Name . New York:: Longmans Green Co.
    [Google Scholar]
  61. 61.
    Goldman DE. 1943.. Potential, impedance, and rectification in membranes. . J. Gen. Physiol. 27::3760
    [Crossref] [Google Scholar]
  62. 62.
    Gouy LG. 1910.. Sur la constitution de la charge électrique a la surface d'un électrolyte. . J. Phys. Théor. Appl. 9::45768
    [Google Scholar]
  63. 63.
    Grabe M, Oster G. 2001.. Regulation of organelle acidity. . J. Gen. Physiol. 117::32944
    [Crossref] [Google Scholar]
  64. 64.
    Groisman EA, Hollands K, Kriner MA, Lee E-J, Park S-Y, Pontes MH. 2013.. Bacterial Mg2+ homeostasis, transport, and virulence. . Annu. Rev. Genet. 47::62546
    [Crossref] [Google Scholar]
  65. 65.
    Guo J, Zhou H-X. 2016.. Protein allostery and conformational dynamics. . Chem. Rev. 116::650315
    [Crossref] [Google Scholar]
  66. 66.
    Gutstein M. 1933.. Bestimmung der H-Konzentration in der lebenden Hefe- und Bakterienzelle. . Protoplasma 17::45470
    [Crossref] [Google Scholar]
  67. 67.
    Hall JE, Mead CA, Szabo G. 1973.. A barrier model for current flow in lipid bilayer membranes. . J. Membr. Biol. 11::7597
    [Crossref] [Google Scholar]
  68. 68.
    Han J, Burgess K. 2010.. Fluorescent indicators for intracellular pH. . Chem. Rev. 110::270928
    [Crossref] [Google Scholar]
  69. 69.
    Häse CC, Fedorova ND, Galperin MY, Dibrov PA. 2001.. Sodium ion cycle in bacterial pathogens: evidence from cross-genome comparisons. . Microbiol. Mol. Biol. Rev. 65::35370
    [Crossref] [Google Scholar]
  70. 70.
    Heimburg T. 2012.. The capacitance and electromechanical coupling of lipid membranes close to transitions: the effect of electrostriction. . Biophys. J. 103::91829
    [Crossref] [Google Scholar]
  71. 71.
    Hille B. 2001.. Ion Channels of Excitable Membranes. Sunderland, MA:: Sinauer Assoc.
    [Google Scholar]
  72. 72.
    Hodgkin AL, Huxley AF. 1939.. Action potentials recorded from inside a nerve fibre. . Nature 144::71011
    [Crossref] [Google Scholar]
  73. 73.
    Hodgkin AL, Huxley AF. 1952.. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. . J. Physiol. 116::44972
    [Crossref] [Google Scholar]
  74. 74.
    Hodgkin AL, Huxley AF. 1952.. A quantitative description of membrane current and its application to conduction and excitation in nerve. . J. Physiol. 117::50044
    [Crossref] [Google Scholar]
  75. 75.
    Imae Y, Atsumi T. 1989.. Na+-driven bacterial flagellar motors. . J. Bioenerg. Biomembr. 21::70516
    [Crossref] [Google Scholar]
  76. 76.
    Jiang Y, Idikuda V, Chanda B. 2021.. Preparation of giant Escherichia coli spheroplasts for electrophysiological recordings. . Bio Protoc. 11::e4261
    [Crossref] [Google Scholar]
  77. 77.
    Jin L, Han Z, Platisa J, Wooltorton JRA, Cohen LB, Pieribone VA. 2012.. Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. . Neuron 75::77985
    [Crossref] [Google Scholar]
  78. 78.
    Jin X, Zhang X, Ding X, Tian T, Tseng C-K, et al. 2023.. Sensitive bacterial Vm sensors revealed the excitability of bacterial Vm and its role in antibiotic tolerance. . PNAS 120::e2208348120
    [Crossref] [Google Scholar]
  79. 79.
    Jindal S, Yang L, Day PJ, Kell DB. 2019.. Involvement of multiple influx and efflux transporters in the accumulation of cationic fluorescent dyes by Escherichia coli. . BMC Microbiol. 19::195
    [Crossref] [Google Scholar]
  80. 80.
    Jones HE, Holland IB, Campbell AK. 2002.. Direct measurement of free Ca2+ shows different regulation of Ca2+ between the periplasm and the cytosol of Escherichia coli. . Cell Calcium 32::18392
    [Crossref] [Google Scholar]
  81. 81.
    Kay AR. 2017.. How cells can control their size by pumping ions. . Front. Cell. Dev. Biol. 8::541
    [Google Scholar]
  82. 82.
    Keener JP, Sneyd J. 2009.. Mathematical Physiology, Vol. I: Cellular Physiology. New York:: Springer
    [Google Scholar]
  83. 83.
    Kikuchi K, Galera-Laporta L, Weatherwax C, Lam JY, Moon EC, et al. 2022.. Electrochemical potential enables dormant spores to integrate environmental signals. . Science 378::4349
    [Crossref] [Google Scholar]
  84. 84.
    King MM, Kayastha BB, Franklin MJ, Patrauchan MA. 2020.. Calcium regulation of bacterial virulence. . Calcium Signal. 1131::82755
    [Crossref] [Google Scholar]
  85. 85.
    Kneen M, Farinas J, Li Y, Verkman AS. 1998.. Green fluorescent protein as a noninvasive intracellular pH indicator. . Biophys. J. 74::159199
    [Crossref] [Google Scholar]
  86. 86.
    Koch A. 1985.. How bacteria grow and divide in spite of internal hydrostatic pressure. . Can. J. Microbiol. 31::107184
    [Crossref] [Google Scholar]
  87. 87.
    Korzeniewski B. 1998.. Regulation of ATP supply during muscle contraction: theoretical studies. . Biochem. J. 330::118995
    [Crossref] [Google Scholar]
  88. 88.
    Korzeniewski B. 2000.. Regulation of ATP supply in mammalian skeletal muscle during resting state intensive work transition. . Biophys. Chem. 83::1934
    [Crossref] [Google Scholar]
  89. 89.
    Kralj JM, Hochbaum DR, Douglass AD, Cohen AE. 2011.. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. . Science 333::34548
    [Crossref] [Google Scholar]
  90. 90.
    Krasnopeeva E. 2019.. Single cell measurements of bacterial physiology traits during exposure to an external stress. PhD Thesis , Univ. Edinburgh. https://era.ed.ac.uk/handle/1842/35514
    [Google Scholar]
  91. 91.
    Krasnopeeva E, Barboza-Perez UE, Rosko J, Pilizota T, Lo C-J. 2021.. Bacterial flagellar motor as a multimodal biosensor. . Methods 193::515
    [Crossref] [Google Scholar]
  92. 92.
    Krasnopeeva E, Lo C-J, Pilizota T. 2019.. Single-cell bacterial electrophysiology reveals mechanisms of stress-induced damage. . Biophys. J. 116::239099
    [Crossref] [Google Scholar]
  93. 93.
    Kurkdjian A, Guern J. 1989.. Intracellular pH: measurement and importance in cell activity. . Annu. Rev. Plant Physiol. Plant Mol. Biol. 40::271303
    [Crossref] [Google Scholar]
  94. 94.
    Langosch D, Arkin IT. 2009.. Interaction and conformational dynamics of membrane-spanning protein helices. . Protein Sci. 18::134358
    [Crossref] [Google Scholar]
  95. 95.
    Läuger P, Stark G. 1970.. Kinetics of carrier-mediated ion transport across lipid bilayer membranes. . Biochim. Biophys. Acta Biomembr. 211::45866
    [Crossref] [Google Scholar]
  96. 96.
    Le D, Krasnopeeva E, Sinjab F, Pilizota T, Kim M. 2021.. Active efflux leads to heterogeneous dissipation of proton motive force by protonophores in bacteria. . mBio 12::e00676-21
    [Crossref] [Google Scholar]
  97. 97.
    Lee W, Kim K-J, Lee DG. 2014.. A novel mechanism for the antibacterial effect of silver nanoparticles on Escherichia coli. . BioMetals 27::1191201
    [Crossref] [Google Scholar]
  98. 98.
    Lele PP, Hosu BG, Berg HC. 2013.. Dynamics of mechanosensing in the bacterial flagellar motor. . PNAS 110::1183944
    [Crossref] [Google Scholar]
  99. 99.
    Li N, Kojima S, Homma M. 2011.. Sodium-driven motor of the polar flagellum in marine bacteria Vibrio: sodium-driven motor of the polar flagellum. . Genes Cells 16::98599
    [Crossref] [Google Scholar]
  100. 100.
    Li Y, Tsien RW. 2012.. pHTomato, a red, genetically encoded indicator that enables multiplex interrogation of synaptic activity. . Nat. Neurosci. 15::104753
    [Crossref] [Google Scholar]
  101. 101.
    Lo C-J, Leake MC, Berry RM. 2006.. Fluorescence measurement of intracellular sodium concentration in single Escherichia coli cells. . Biophys. J. 90::35765
    [Crossref] [Google Scholar]
  102. 102.
    Lo C-J, Leake MC, Pilizota T, Berry RM. 2007.. Nonequivalence of membrane voltage and ion-gradient as driving forces for the bacterial flagellar motor at low load. . Biophys. J. 93::294302
    [Crossref] [Google Scholar]
  103. 103.
    Lund PA, De Biase D, Liran O, Scheler O, Mira NP, et al. 2020.. Understanding how microorganisms respond to acid pH is central to their control and successful exploitation. . Front. Microbiol. 11::556140
    [Crossref] [Google Scholar]
  104. 104.
    Maex R. 2014.. Nernst-Planck equation. . In Encyclopedia of Computational Neuroscience, ed. D Jaeger, R Jung . New York:: Springer. https://doi.org/10.1007/978-1-4614-7320-6_233-1
    [Google Scholar]
  105. 105.
    Maffeo C, Bhattacharya S, Yoo J, Wells D, Aksimentiev A. 2012.. Modeling and simulation of ion channels. . Chem. Rev. 112::625084
    [Crossref] [Google Scholar]
  106. 106.
    Magge A, Setlow B, Cowan AE, Setlow P. 2009.. Analysis of dye binding by and membrane potential in spores of Bacillus species. . J. Appl. Microbiol. 106::81424
    [Crossref] [Google Scholar]
  107. 107.
    Magnus G, Keizer J. 1997.. Minimal model of beta-cell mitochondrial Ca2+ handling. . Am. J. Physiol. 273::C71733
    [Crossref] [Google Scholar]
  108. 108.
    Maher MP, Wu N-T, Ao H. 2007.. pH-insensitive FRET voltage dyes. . SLAS Discov. 12::65667
    [Crossref] [Google Scholar]
  109. 109.
    Mancini L, Terradot G, Tian T, Pu Y, Li Y, et al. 2020.. A general workflow for characterization of Nernstian dyes and their effects on bacterial physiology. . Biophys. J. 118::414
    [Crossref] [Google Scholar]
  110. 110.
    Mandadapu KK, Nirody JA, Berry RM, Oster G. 2015.. Mechanics of torque generation in the bacterial flagellar motor. . PNAS 112::E438189
    [Crossref] [Google Scholar]
  111. 111.
    Martinez KA, Kitko RD, Mershon JP, Adcox HE, Malek KA, et al. 2012.. Cytoplasmic pH response to acid stress in individual cells of Escherichia coli and Bacillus subtilis observed by fluorescence ratio imaging microscopy. . Appl. Environ. Microbiol. 78::370614
    [Crossref] [Google Scholar]
  112. 112.
    Marx D. 2006.. Proton transfer 200 years after von Grotthuss: insights from ab initio simulations. . ChemPhysChem 7::184870
    [Crossref] [Google Scholar]
  113. 113.
    Matlashov ME, Bogdanova YA, Ermakova GV, Mishina NM, Ermakova YG, et al. 2015.. Fluorescent ratiometric pH indicator SypHer2: applications in neuroscience and regenerative biology. . Biochim. Biophys. Acta Gen. Subj. 1850::231828
    [Crossref] [Google Scholar]
  114. 114.
    McLaughlin S. 1989.. The electrostatic properties of membranes. . Annu. Rev. Biophys. Biophys. Chem. 18::11336
    [Crossref] [Google Scholar]
  115. 115.
    Miesenbock G, De Angelis DA, Rothman JE. 1998.. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. . Nature 394::19295
    [Crossref] [Google Scholar]
  116. 116.
    Mitchell P. 1961.. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. . Nature 191::14448
    [Crossref] [Google Scholar]
  117. 117.
    Moon RB, Richards JH. 1973.. Determination of intracellular pH by 31P magnetic resonance. . J. Biol. Chem. 248::727678
    [Crossref] [Google Scholar]
  118. 118.
    Mulkidjanian AY, Dibrov P, Galperin MY. 2008.. The past and present of sodium energetics: May the sodium-motive force be with you. . Biochim. Biophys. Acta Bioenerg. 1777:(7–8):98592
    [Crossref] [Google Scholar]
  119. 119.
    Nagata S, Adachi K, Shirai K, Sano H. 1995.. 23Na NMR spectroscopy of free Na+ in the halotolerant bacterium Brevibacterium sp. and Escherichia coli. . Microbiology 141::72936
    [Crossref] [Google Scholar]
  120. 120.
    Nernst W. 1888.. Zur Kinetik der in Lösung befindlichen Körper. . Z. Phys. Chem. 2::61337
    [Crossref] [Google Scholar]
  121. 121.
    Nernst W. 1889.. Die elektromotorische Wirksamkeit der Jonen. . Z. Phys. Chem. 4::12981
    [Crossref] [Google Scholar]
  122. 122.
    Nirody JA, Sun Y-R, Lo C-J. 2017.. The biophysicist's guide to the bacterial flagellar motor. . Adv. Phys. X 2::32443
    [Google Scholar]
  123. 123.
    Nord AL, Gachon E, Perez-Carrasco R, Nirody JA, Barducci A, et al. 2017.. Catch bond drives stator mechanosensitivity in the bacterial flagellar motor. . PNAS 114::1295257
    [Crossref] [Google Scholar]
  124. 124.
    Norris V, Grant S, Freestone P, Canvin J, Sheikh FN, et al. 1996.. Calcium signalling in bacteria. . J. Bacteriol. 178::367782
    [Crossref] [Google Scholar]
  125. 125.
    Oldham KB. 2008.. A Gouy-Chapman-Stern model of the double layer at a (metal)/(ionic liquid) interface. . J. Electroanal. Chem. 613::13138
    [Crossref] [Google Scholar]
  126. 126.
    Parry BR, Surovtsev IV, Cabeen MT, O'Hern CS, Dufresne ER, Jacobs-Wagner C. 2014.. The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. . Cell 156:(1–2):18394
    [Crossref] [Google Scholar]
  127. 127.
    Petsev DN, Van Swol F, Frink LJD. 2021.. Molecular Theory of Electric Double Layers. Bristol, UK:: IoP Publ.
    [Google Scholar]
  128. 128.
    Pickard WF. 1976.. Generalizations of the Goldman-Hodgkin-Katz equation. . Math. Biosci. 30::99111
    [Crossref] [Google Scholar]
  129. 129.
    Planck M. 1890.. Über die Erregung von Elektricität und Wärme in Elektrolyten. . Wied. Ann. Phys. 39::16186
    [Crossref] [Google Scholar]
  130. 130.
    Poolman B, Knol J, Van Der Does C, Henderson PJF, Liang W-J, et al. 1996.. Cation and sugar selectivity determinants in a novel family of transport proteins. . Mol. Microbiol. 19::91122
    [Crossref] [Google Scholar]
  131. 131.
    Prats M, Tocanne JF, Teissie J. 1987.. Lateral proton conduction at a lipid/water interface. Effect of lipid nature and ionic content of the aqueous phase. . Eur. J. Biochem. 162:(2):37985
    [Crossref] [Google Scholar]
  132. 132.
    Prindle A, Liu J, Asally M, Ly S, Garcia-Ojalvo J, Süel GM. 2015.. Ion channels enable electrical communication in bacterial communities. . Nature 527::5963
    [Crossref] [Google Scholar]
  133. 133.
    Prodan C, Prodan E. 1999.. The dielectric behaviour of living cell suspensions. . J. Phys. D 32::33543
    [Crossref] [Google Scholar]
  134. 134.
    Prodan E, Prodan C, Miller JH. 2008.. The dielectric response of spherical live cells in suspension: an analytic solution. . Biophys. J. 95::417482
    [Crossref] [Google Scholar]
  135. 135.
    Ramahi AA, Ruff RL. 2014.. Membrane potential. . In Encyclopedia of the Neurological Sciences, ed. MJ Aminoff, RB Daroff , pp. 103435. Amsterdam:: Elsevier. , 2nd ed..
    [Google Scholar]
  136. 136.
    Ramirez N, Regueiro A, Arias O, Contreras R. 2009.. Electrochemical impedance spectroscopy: an effective tool for a fast microbiological diagnosis. . Biotecnol. Apl. 26::7278
    [Google Scholar]
  137. 137.
    Rana PS, Gibbons BA, Vereninov AA, Yurinskaya VE, Clements RJ, et al. 2019.. Calibration and characterization of intracellular Asante Potassium Green probes, APG-2 and APG-4. . Anal. Biochem. 567::813
    [Crossref] [Google Scholar]
  138. 138.
    Reeve JE, Corbett AD, Boczarow I, Kaluza W, Barford W, et al. 2013.. Porphyrins for probing electrical potential across lipid bilayer membranes by second harmonic generation. . Angew. Chem. Int. Ed. 52::904448
    [Crossref] [Google Scholar]
  139. 139.
    Reid SW, Leake MC, Chandler JH, Lo C-J, Armitage JP, Berry RM. 2006.. The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11. . PNAS 103::806671
    [Crossref] [Google Scholar]
  140. 140.
    Robey RB, Ruiz O, Santos AVP, Ma J, Kear F, et al. 1998.. pH-dependent fluorescence of a heterologously expressed Aequorea green fluorescent protein mutant: in situ spectral characteristics and applicability to intracellular pH estimation. . Biochemistry 37::9894901
    [Crossref] [Google Scholar]
  141. 141.
    Rose L, Jenkins ATA. 2007.. The effect of the ionophore valinomycin on biomimetic solid supported lipid DPPTE/EPC membranes. . Bioelectrochemistry 70::38793
    [Crossref] [Google Scholar]
  142. 142.
    Salcedo-Sora JE, Jindal S, O'Hagan S, Kell DB. 2021.. A palette of fluorophores that are differentially accumulated by wild-type and mutant strains of Escherichia coli: surrogate ligands for profiling bacterial membrane transporters. . Microbiology 167::001016
    [Crossref] [Google Scholar]
  143. 143.
    Savtchenko LP, Poo MM, Rusakov DA. 2017.. Electrodiffusion phenomena in neuroscience: a neglected companion. . Nat. Rev. Neurosci. 18::598612
    [Crossref] [Google Scholar]
  144. 144.
    Schink S, Polk M, Athaide E, Mukherjee A, Ammar C, et al. 2021.. Electrodiffusion phenomena in neuroscience: a neglected companion. . bioRxiv 2021.11.22.469587. https://doi.org/10.1101/2021.11.22.469587
  145. 145.
    Schmidt A, Kochanowski K, Vedelaar S, Ahrné E, Volkmer B, et al. 2016.. The quantitative and condition-dependent Escherichia coli proteome. . Nat. Biotechnol. 34::10410
    [Crossref] [Google Scholar]
  146. 146.
    Schwarz J, Schumacher K, Brameyer S, Jung K. 2022.. Bacterial battle against acidity. . FEMS Microbiol. Rev. 46::fuac037
    [Crossref] [Google Scholar]
  147. 147.
    Schwarz-Linek J, Arlt J, Jepson A, Dawson A, Vissers T, et al. 2016.. Escherichia coli as a model active colloid: a practical introduction. . Colloids Surf. B 137::216
    [Crossref] [Google Scholar]
  148. 148.
    Schwarzlander M, Wagner S, Ermakova YG, Belousov VV, Radi R, et al. 2014.. The “mitoflash” probe cpYFP does not respond to superoxide. . Nature 514::E1214
    [Crossref] [Google Scholar]
  149. 149.
    Schwiening C. 1999.. Measurement of intracellular pH: a comparison between ion-sensitive microelectrodes and fluorescent dyes. . In Regulation of Tissue pH in Plants and Animals: A Reappraisal of Current Techniques, ed. S Egginton, EW Taylor, JA Raven , pp. 118. Cambridge, UK:: Cambridge Univ. Press
    [Google Scholar]
  150. 150.
    Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, Tsien RY. 2004.. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. . Nat. Biotechnol. 22::156772
    [Crossref] [Google Scholar]
  151. 151.
    Sigworth FJ. 1980.. The variance of sodium current fluctuations at the node of Ranvier. . J. Physiol. 307::97129
    [Crossref] [Google Scholar]
  152. 152.
    Sirec T, Benarroch JM, Buffard P, Garcia-Ojalvo J, Asally M. 2019.. Electrical polarization enables integrative quality control during bacterial differentiation into spores. . iScience 16::37889
    [Crossref] [Google Scholar]
  153. 153.
    Skulachev VP. 1978.. Membrane-linked energy buffering as the biological function of Na+/K+ gradient. . FEBS Lett. 87::17179
    [Crossref] [Google Scholar]
  154. 154.
    Skulachev VP. 1985.. Membrane-linked energy transductions. Bioenergetic functions of sodium: H+ is not unique as a coupling ion. . Eur. J. Biochem. 151::199208
    [Crossref] [Google Scholar]
  155. 155.
    Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA. 2009.. Cytoplasmic pH measurement and homeostasis in bacteria and archaea. . Adv. Microb. Physiol. 55::179
    [Crossref] [Google Scholar]
  156. 156.
    Sowa Y, Berry RM. 2008.. Bacterial flagellar motor. . Q. Rev. Biophys. 41::10332
    [Crossref] [Google Scholar]
  157. 157.
    Sowa Y, Homma M, Ishijima A, Berry RM. 2014.. Hybrid-fuel bacterial flagellar motors in Escherichia coli. . PNAS 111::343641
    [Crossref] [Google Scholar]
  158. 158.
    Sowa Y, Hotta H, Homma M, Ishijima A. 2003.. Torque–speed relationship of the Na+-driven flagellar motor of Vibrio alginolyticus. . J. Mol. Biol. 327::104351
    [Crossref] [Google Scholar]
  159. 159.
    Stern O. 1924.. Zur Theorie der elektrolytischen Doppelschicht. . Z. Elektrochem. Angew. Phys. Chem. 30::50816
    [Google Scholar]
  160. 160.
    Stock J, Roseman S. 1971.. A sodium-dependent sugar co-transport system in bacteria. . Biochem. Biophys. Res. Commun. 44::13238
    [Crossref] [Google Scholar]
  161. 161.
    Stratford JP, Edwards CLA, Ghanshyam MJ, Malyshev D, Delise MA, et al. 2019.. Electrically induced bacterial membrane-potential dynamics correspond to cellular proliferation capacity. . PNAS 116::955257
    [Crossref] [Google Scholar]
  162. 162.
    Szatmári D, Sárkány P, Kocsis B, Nagy T, Miseta A, et al. 2020.. Intracellular ion concentrations and cation-dependent remodelling of bacterial MreB assemblies. . Sci. Rep. 10::12002
    [Crossref] [Google Scholar]
  163. 163.
    Takeuchi A, Takeuchi N. 1960.. On the permeability of end-plate membrane during the action of transmitter. . J. Physiol. 154::5267
    [Crossref] [Google Scholar]
  164. 164.
    Takeuchi N. 1963.. Effects of calcium on the conductance change of the end-plate membrane during the action of transmitter. . J. Physiol. 167::14155
    [Crossref] [Google Scholar]
  165. 165.
    Takeuchi N. 1963.. Some properties of conductance changes at the end-plate membrane during the action of acetylcholine. . J. Physiol. 167::12840
    [Crossref] [Google Scholar]
  166. 166.
    Tanak Y. 2007.. Membrane characteristics and transport phenomena. . In Ion Exchange Membranes: Fundamentals and Applications, pp. 3757. Membr. Sci. Technol. 12 . Amsterdam:: Elsevier
    [Google Scholar]
  167. 167.
    Tapley TL, Franzmann TM, Chakraborty S, Jakob U, Bardwell JCA. 2010.. Protein refolding by pH-triggered chaperone binding and release. . PNAS 107::107176
    [Crossref] [Google Scholar]
  168. 168.
    Te Winkel JD, Gray DA, Seistrup KH, Hamoen LW, Strahl H. 2016.. Analysis of antimicrobial-triggered membrane depolarization using voltage sensitive dyes. . Front. Cell Dev. Biol. 4::29
    [Crossref] [Google Scholar]
  169. 169.
    Teorell T. 1953.. Transport processes and electrical phenomena in ionic membranes. . Prog. Biophys. Biophys. Chem. 3::30569
    [Crossref] [Google Scholar]
  170. 170.
    Terradot G, Krasnopeeva E, Swain PS, Pilizota T. 2021.. The proton motive force determines Escherichia coli’s robustness to extracellular pH. . bioRxiv 2021.11.19.469321. https://doi.org/10.1101/2021.11.19.469321
  171. 171.
    Tipping MJ, Delalez NJ, Lim R, Berry RM, Armitage JP. 2013.. Load-dependent assembly of the bacterial flagellar motor. . mBio 4::e00551-13
    [Crossref] [Google Scholar]
  172. 172.
    Tisa LS, Adler J. 1995.. Cytoplasmic free-Ca2+ level rises with repellents and falls with attractants in Escherichia coli chemotaxis. . PNAS 92::1077781
    [Crossref] [Google Scholar]
  173. 173.
    Torrecilla I, Leganés F, Bonilla I, Fernández-Piñas F. 2000.. Use of recombinant aequorin to study calcium homeostasis and monitor calcium transients in response to heat and cold shock in cyanobacteria. . Plant Physiol. 123::16176
    [Crossref] [Google Scholar]
  174. 173a.
    Tosteson DC, Hoffman JF. 1960.. Regulation of cell volume by active cation transport in high and low potassium sheep red cells. . J. Gen. Physiol. 44:(1):16994
    [Crossref] [Google Scholar]
  175. 174.
    Unden G, Becker S, Bongaerts J, Schirawski J, Six S. 1994.. Oxygen regulated gene expression in facultatively anaerobic bacteria. . Antonie Van Leeuwenhoek 66::322
    [Crossref] [Google Scholar]
  176. 175.
    van Rotterdam BJ, Crielaard W, van Stokkum IHM, Hellingwerf KJ, Westerhoff HV. 2002.. Simplicity in complexity: the photosynthetic reaction center performs as a simple 0.2 V battery. . FEBS Lett. 510::1057
    [Crossref] [Google Scholar]
  177. 176.
    Walter JM, Greenfield D, Bustamante C, Liphardt J. 2007.. Light-powering Escherichia coli with proteorhodopsin. . PNAS 104::240812
    [Crossref] [Google Scholar]
  178. 177.
    Wang F, Qin L, Pace CP, Wong P, Malonis R, Gao J. 2012.. Solubilized gramicidin A as potential systemic antibiotics. . ChemBioChem 13::5155
    [Crossref] [Google Scholar]
  179. 178.
    Wang Y, Krasnopeeva E, Lin S, Bai F, Pilizota T, Lo C. 2019.. Comparison of Escherichia coli surface attachment methods for single-cell microscopy. . Sci. Rep. 9::19418
    [Crossref] [Google Scholar]
  180. 179.
    Watkins NJ, Knight MR, Trewavas AJ, Campbell AK. 1995.. Free calcium transients in chemotactic and non-chemotactic strains of Escherichia coli determined by using recombinant aequorin. . Biochem. J. 306::86569
    [Crossref] [Google Scholar]
  181. 180.
    Wendel BM, Pi H, Krüger L, Herzberg C, Stülke J, Helmann JD. 2022.. A central role for magnesium homeostasis during adaptation to osmotic stress. . mBio 13::e00092-22
    [Crossref] [Google Scholar]
  182. 181.
    White SH. 1970.. A study of lipid bilayer membrane stability using precise measurements of specific capacitance. . Biophys. J. 10::112748
    [Crossref] [Google Scholar]
  183. 182.
    Williams JA. 1970.. Origin of transmembrane potentials in non-excitable cells. . J. Theor. Biol. 28::28796
    [Crossref] [Google Scholar]
  184. 183.
    Wilson TH, Ding PZ. 2001.. Sodium-substrate cotransport in bacteria. . Biochim. Biophys. Acta Bioenerg. 1505::12130
    [Crossref] [Google Scholar]
  185. 184.
    Wood JM. 2007.. Bacterial osmosensing transporters. . Methods Enzymol. 428::77107
    [Crossref] [Google Scholar]
  186. 185.
    Wright MR. 2007.. An Introduction to Aqueous Electrolyte Solutions. Hoboken, NJ:: Wiley
    [Google Scholar]
  187. 186.
    Zarbiv G, Li H, Wolf A, Cecchini G, Caplan SR, et al. 2012.. Energy complexes are apparently associated with the switch-motor complex of bacterial flagella. . J. Mol. Biol. 416:(2):192207
    [Crossref] [Google Scholar]
  188. 187.
    Zhang F, Wang S, Yang Y, Jiang J, Tao N. 2021.. Imaging single bacterial cells with electro-optical impedance microscopy. . ACS Sens. 6::34854
    [Crossref] [Google Scholar]
  189. 188.
    Zilberstein D, Agmon V, Schuldiner S, Padan E. 1984.. Escherichia coli intracellular pH, membrane potential, and cell growth. . J. Bacteriol. 158::24652
    [Crossref] [Google Scholar]
  190. 189.
    Zochowski M, Wachowiak M, Falk CX, Cohen LB, Lam YW, et al. 2000.. Imaging membrane potential with voltage-sensitive dyes. . Biol. Bull. 198::121
    [Crossref] [Google Scholar]
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