Ion channels enable electrical communication in bacterial communities

Nature

Volumn 527, Issue 7576, 2015, Pages 59-63

  Prindle, Arthur ^a   Liu, Jintao ^a   Asally, Munehiro ^b   Ly, San ^a   Garcia Ojalvo, Jordi ^c   Süel, Gürol M ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; POTASSIUM; POTASSIUM CHANNEL;

BACTERIUM; BIOFILM; CELLS AND CELL COMPONENTS; ELECTRICAL CONDUCTIVITY; ION EXCHANGE; IONIC COMPOSITION; METABOLISM; MICROBIAL COMMUNITY; NEUROLOGY; NUMERICAL MODEL; POTASSIUM; WAVE PROPAGATION;

ARTICLE; BIOFILM; CELL METABOLISM; CHANNEL GATING; DEPOLARIZATION; ELECTRICAL PARAMETERS; INTRACELLULAR SIGNALING; MATHEMATICAL MODEL; MICROBIAL COMMUNITY; NONHUMAN; POSITIVE FEEDBACK; POTASSIUM CELL LEVEL; PRIORITY JOURNAL; PROKARYOTIC CELL; BACILLUS SUBTILIS; BIOLOGICAL MODEL; CYTOLOGY; ELECTRIC CONDUCTIVITY; FEEDBACK SYSTEM; GROWTH, DEVELOPMENT AND AGING; MEMBRANE POTENTIAL; METABOLISM; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PROKARYOTA;

BACILLUS SUBTILIS; BIOFILMS; ELECTRIC CONDUCTIVITY; FEEDBACK, PHYSIOLOGICAL; ION CHANNEL GATING; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; POTASSIUM; POTASSIUM CHANNELS; SIGNAL TRANSDUCTION;

EID: 84946221763     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature15709     Document Type: Article

References (50)

1. Gerstner, W. & Kistler, W. M. Spiking Neuron Models: Single Neurons, Populations, Plasticity (Cambridge Univ. Press, 2002).
2. Hille, B. Ion Channels of Excitable Membranes (Sinauer Associates, 2001).
3. MacKinnon, R. Potassium channels and the atomic basis of selective ion conduction. Biosci. Rep. 24, 75-100 (2004).
4. Doyle, D. A. et al. The structure of the potassium channel: molecular basis of K1 conduction and selectivity. Science 280, 69-77 (1998).
5. Ren, D. et al. A prokaryotic voltage-gated sodium channel. Science 294, 2372-2375 (2001).
6. Iyer, R., Iverson, T. M., Accardi, A. & Miller, C. A biological role for prokaryotic ClC chloride channels. Nature 419, 715-718 (2002).
7. Jiang, Y. et al. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417, 515-522 (2002).
8. Chen, G. Q., Cui, C., Mayer, M. L. & Gouaux, E. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402, 817-821 (1999).
9. Kuo, M. M. C., Haynes, W. J., Loukin, S. H., Kung, C. & Saimi, Y. Prokaryotic K1 channels: From crystal structures to diversity. FEMS Microbiol. Rev. 29, 961-985 (2005).
10. Saimi, Y., Loukin, S. H., Zhou, X. L., Martinac, B. &Kung, C. Ion channels inmicrobes. Methods Enzymol. 294, 507-524 (1998).
11. Martinac, B., Buechner, M., Delcour, A. H., Adler, J. &Kung, C. Pressure-sensitive ion channel in Escherichia coli. Proc. Natl Acad. Sci. USA 84, 2297-2301 (1987).
12. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: A common cause of persistent infections. Science 284, 1318-1322 (1999).
13. Hall-Stoodley, L., Costerton, J. W. &Stoodley, P. Bacterial biofilms: fromthe natural environment to infectious diseases. Nature Rev. Microbiol. 2, 95-108 (2004).
14. Vlamakis, H., Aguilar, C., Losick, R. & Kolter, R. Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev. 22, 945-953 (2008).
15. Asally, M. et al. Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc. Natl Acad. Sci. USA 109, 18891-18896 (2012).
16. Wilking, J. N. et al. Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proc. Natl Acad. Sci. USA 110, 848-852 (2013).
17. Payne, S. et al. Temporal control of self-organized pattern formation without morphogen gradients in bacteria. Mol. Syst. Biol. 9, 697 (2013).
18. Liu, J. et al. Metabolic co-dependence gives rise to collective oscillations within microbial communities. Nature 523, 550-554 (2015).
19. Tolner, B., Ubbink-Kok, T., Poolman, B. & Konings, W. N. Characterization of the proton/glutamate symport protein of Bacillus subtilis and its functional expression in Escherichia coli. J. Bacteriol. 177, 2863-2869 (1995).
20. Boogerd, F. C. et al. AmtB-mediated NH3 transport in prokaryotes must be active and as a consequence regulation of transport by GlnK is mandatory to limit futile cycling of NH4 1/NH3. FEBS Lett. 585, 23-28 (2011).
21. Kralj, J. M., Hochbaum, D. R., Douglass, A. D. & Cohen, A. E. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333, 345-348 (2011).
22. Lo, C.-J., Leake, M. C., Pilizota, T. & Berry, R. M. Nonequivalence of membrane voltage and ion-gradient as driving forces for the bacterial flagellar motor at low load. Biophys. J. 93, 294-302 (2007).
23. Strahl, H. & Hamoen, L. W. Membrane potential is important for bacterial cell division. Proc. Natl Acad. Sci. USA 107, 12281-12286 (2010).
24. Krulwich, T. A., Sachs, G. &Padan, E. Molecular aspects of bacterial pHsensing and homeostasis. Nature Rev. Microbiol. 9, 330-343 (2011).
25. Epstein, W. The roles and regulation of potassium in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 75, 293-320 (2003).
26. López, D., Fischbach, M. A., Chu, F., Losick, R. & Kolter, R. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl Acad. Sci. USA 106, 280-285 (2009).
27. Kinsinger, R. F., Kearns, D. B., Hale, M. &Fall, R. Genetic requirements for potassium ion-dependent colony spreading in Bacillus subtilis. J. Bacteriol. 187, 8462-8469 (2005).
28. Vieira-Pires, R. S., Szollosi, A. & Morais-Cabral, J. H. The structure of the KtrAB potassium transporter. Nature 496, 323-328 (2013).
29. Holtmann, G., Bakker, E. P., Uozumi, N. & Bremer, E. KtrAB and KtrCD: Two K1 uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity. J. Bacteriol. 185, 1289-1298 (2003).
30. Whatmore, A. M., Chudek, J. A. & Reed, R. H. The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J. Gen. Microbiol. 136, 2527-2535 (1990).
31. Rimmele, T. S. & Chatton, J. Y. A novel optical intracellular imaging approach for potassium dynamics in astrocytes. PLoS ONE 9, 1-9 (2014).
32. Margolin, Y. & Eisenbach, M. Voltage clamp effects on bacterial chemotaxis. J. Bacteriol. 159, 605-610 (1984).
33. Lundberg, M. E., Becker, E. C. & Choe, S. MstX and a putative potassium channel facilitate biofilm formation in Bacillus subtilis. PLoS ONE 8, e60993 (2013).
34. Cao, Y. et al. Gating of the TrkH ion channel by its associated RCK protein TrkA. Nature 496, 317-322 (2013).
35. Roosild, T. P., Miller, S., Booth, I. R. & Choe, S. A mechanism of regulating transmembrane potassium flux through a ligand-mediated conformational switch. Cell 109, 781-791 (2002).
36. Schlosser, A., Hamann, A., Bossemeyer, D., Schneider, E. & Bakker, E. P. NAD1 binding to the Escherichia coli K1-uptake protein TrkA and sequence similarity between TrkA anddomains of a family of dehydrogenases suggest a role for NAD1 in bacterial transport. Mol. Microbiol. 9, 533-543 (1993).
37. Fisher, S. H. Regulation of nitrogen metabolism in Bacillus subtilis: vive la différence! Mol. Microbiol. 32, 223-232 (1999).
38. Cortes, D. M., Cuello, L. G. & Perozo, E. Molecular architecture of full-length KcsA: role of cytoplasmic domains in ion permeation and activation gating. J. Gen. Physiol. 117, 165-180 (2001).
39. Hodgkin, A. L. & Huxley, A. F. A quantitative description ofmembrane current and its applications to conduction and excitation in nerve. J. Physiol. (Lond.) 117, 500-544 (1952).
40. Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346 (2005).
41. Kato, S., Hashimoto, K. & Watanabe, K. Iron-oxide minerals affect extracellular electron-transfer paths of Geobacter spp. Microbes Environ. 28, 141-148 (2013).
42. Pfeffer, C. et al. Filamentous bacteria transport electrons over centimetre distances. Nature 491, 218-221 (2012).
43. Masi, E. et al. Electrical spiking in bacterial biofilms. J. R. Soc. Interface 12, 1-10 (2014).
44. Pan, J. W. et al. Neurometabolismin human epilepsy. Epilepsia 49, 31-41 (2008).
45. Petroff, O. A. C., Errante, L. D., Rothman, D. L., Kim, J. H. & Spencer, D. D. Glutamateglutamine cycling in the epileptic human hippocampus. Epilepsia 43, 703-710 (2002).
46. Meldrum, B. S. Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J. Nutr. 130, 1007S-1015S (2000).
47. Irnov, I. & Winkler, W. C. A regulatory RNA required for antitermination of biofilm and capsular polysaccharide operons in Bacillales. Mol. Microbiol. 76, 559-575 (2010).
48. Jarmer, H., Berka, R., Knudsen, S. & Saxild, H. H. Transcriptome analysis documents induced competence of Bacillus subtilis during nitrogen limiting conditions. FEMS Microbiol. Lett. 206, 197-200 (2002).
49. Horvath, A. L. Handbook of Aqueous Electrolyte Solutions: Physical Properties, Estimation and Correlation Methods (Ellis Horwood Ltd, 1985).
50. Stewart, P. S. Diffusion in biofilms. J. Bacteriol. 185, 1485-1491 (2003).