Species-Independent Attraction to Biofilms through Electrical Signaling

Cell

Volumn 168, Issue 1-2, 2017, Pages 200-209.e12

  Humphries, Jacqueline ^a   Xiong, Liyang ^b   Liu, Jintao ^a   Prindle, Arthur ^a   Yuan, Fang ^a   Arjes, Heidi A ^c,d   Tsimring, Lev ^e,f   Süel, Gürol M ^a,e,f,g  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Stanford University   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f University of California San Diego   (United States)

^g UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

bacterial communities; biofilm; electrical signaling; ion channel; long range signaling; membrane potential; motility; multispecies; single cell trajectories; tumbling frequency

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BIOFILM; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; ELECTRIC ACTIVITY; MATHEMATICAL MODEL; MICROFLUIDICS; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; CLASSIFICATION; ELECTROPHYSIOLOGY; MEMBRANE POTENTIAL; METABOLISM; MICROFLUIDIC ANALYSIS; PHYSIOLOGY;

BACILLUS SUBTILIS; BIOFILMS; ELECTROPHYSIOLOGICAL PHENOMENA; MEMBRANE POTENTIALS; MICROFLUIDIC ANALYTICAL TECHNIQUES; MODELS, BIOLOGICAL; POTASSIUM; PSEUDOMONAS AERUGINOSA;

EID: 85009209177     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.12.014     Document Type: Article

References (45)

1. Abee, T., Hellingwerf, K.J., Konings, W.N., Effects of potassium ions on proton motive force in Rhodobacter sphaeroides. J. Bacteriol. 170 (1988), 5647–5653.
2. Bakker, E.P., Mangerich, W.E., Interconversion of components of the bacterial proton motive force by electrogenic potassium transport. J. Bacteriol. 147 (1981), 820–826.
3. Berg, H.C., Brown, D.A., Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239 (1972), 500–504.
4. Booth, I.R., Regulation of cytoplasmic pH in bacteria. Microbiol. Rev. 49 (1985), 359–378.
5. Brameyer, S., Bode, H.B., Heermann, R., Languages and dialects: bacterial communication beyond homoserine lactones. Trends Microbiol. 23 (2015), 521–523.
6. Cao, Y., Pan, Y., Huang, H., Jin, X., Levin, E.J., Kloss, B., Zhou, M., Gating of the TrkH ion channel by its associated RCK protein TrkA. Nature 496 (2013), 317–322.
7. Castañeda-García, A., Do, T.T., Blázquez, J., The K+ uptake regulator TrkA controls membrane potential, pH homeostasis and multidrug susceptibility in Mycobacterium smegmatis. J. Antimicrob. Chemother. 66 (2011), 1489–1498.
8. Continuum Analytics (2016). Anaconda. https://www.continuum.io/.
9. De Jong, M.H., van der Drift, C., Vogels, G.D., Proton-motive force and the motile behavior of Bacillus subtilis. Arch. Microbiol. 111 (1976), 7–11.
10. Doyle, D.A., Morais Cabral, J., Pfuetzner, R.A., Kuo, A., Gulbis, J.M., Cohen, S.L., Chait, B.T., MacKinnon, R., The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280 (1998), 69–77.
11. Fell, C.J.D., Hutchison, H.P., Diffusion coefficients for sodium and potassium chlorides in water at elevated temperatures. J. Chem. Eng. Data 16 (1971), 427–429.
12. Gries, C.M., Bose, J.L., Nuxoll, A.S., Fey, P.D., Bayles, K.W., The Ktr potassium transport system in Staphylococcus aureus and its role in cell physiology, antimicrobial resistance and pathogenesis. Mol. Microbiol. 89 (2013), 760–773.
13. Hille, B., Ion Channels of Excitable Membranes. Third Edition, 2001, Sinauer Associates.
14. Hodgkin, A.L., Huxley, A.F., A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117 (1952), 500–544.
15. Irnov, I., Winkler, W.C., A regulatory RNA required for antitermination of biofilm and capsular polysaccharide operons in Bacillales. Mol. Microbiol. 76 (2010), 559–575.
16. 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 (2002), 197–200.
17. Liu, J., Prindle, A., Humphries, J., Gabalda-Sagarra, M., Asally, M., Lee, D.Y., Ly, S., Garcia-Ojalvo, J., Süel, G.M., Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature 523 (2015), 550–554.
18. 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 (2007), 294–302.
19. Lundberg, M.E., Becker, E., Choe, S., MstX and a putative potassium channel facilitate biofilm formation in Bacillus subtilis. PLoS ONE, 8, 2013, e60993.
20. Magnuson, R., Solomon, J., Grossman, A.D., Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77 (1994), 207–216.
21. Manson, M.D., Tedesco, P., Berg, H.C., Harold, F.M., Van der Drift, C., A protonmotive force drives bacterial flagella. Proc. Natl. Acad. Sci. USA 74 (1977), 3060–3064.
22. Mather, W., Mondragón-Palomino, O., Danino, T., Hasty, J., Tsimring, L.S., Streaming instability in growing cell populations. Phys. Rev. Lett., 104, 2010, 208101.
23. MathWorks. (2012). MATLAB and Image Processing Toolkit. https://www.mathworks.com/products/matlab/html.
24. Matsuura, S., Shioi, J.I., Imae, Y., Iida, S., Characterization of the Bacillus subtilis motile system driven by an artificially created proton motive force. J. Bacteriol. 140 (1979), 28–36.
25. Meister, M., Lowe, G., Berg, H.C., The proton flux through the bacterial flagellar motor. Cell 49 (1987), 643–650.
26. Meister, M., Caplan, S.R., Berg, H.C., Dynamics of a tightly coupled mechanism for flagellar rotation. Bacterial motility, chemiosmotic coupling, protonmotive force. Biophys. J. 55 (1989), 905–914.
27. Miller, M.B., Bassler, B.L., Quorum sensing in bacteria. Annu. Rev. Microbiol. 55 (2001), 165–199.
28. Miller, J.B., Koshland, D.E. Jr., Sensory electrophysiology of bacteria: relationship of the membrane potential to motility and chemotaxis in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 74 (1977), 4752–4756.
29. Miller, J.B., Koshland, D.E. Jr., Protonmotive force and bacterial sensing. J. Bacteriol. 141 (1980), 26–32.
30. Paintdakhi, A., Parry, B., Campos, M., Irnov, I., Elf, J., Surovtsev, I., Jacobs-Wagner, C., Oufti: an integrated software package for high-accuracy, high-throughput quantitative microscopy analysis. Mol. Microbiol. 99 (2016), 767–777.
31. Perego, M., Higgins, C.F., Pearce, S.R., Gallagher, M.P., Hoch, J.A., The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol. Microbiol. 5 (1991), 173–185.
32. Plásek, J., Sigler, K., Slow fluorescent indicators of membrane potential: a survey of different approaches to probe response analysis. J. Photochem. Photobiol. B 33 (1996), 101–124.
33. Preibisch, S., Saalfeld, S., Tomancak, P., Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25 (2009), 1463–1465.
34. Prindle, A., Liu, J., Asally, M., Ly, S., Garcia-Ojalvo, J., Süel, G.M., Ion channels enable electrical communication in bacterial communities. Nature 527 (2015), 59–63.
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 (2002), 781–791.
36. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
37. Schlösser, A., Hamann, A., Bossemeyer, D., Schneider, E., Bakker, E.P., NAD+ binding to the Escherichia coli K(+)-uptake protein TrkA and sequence similarity between TrkA and domains of a family of dehydrogenases suggest a role for NAD+ in bacterial transport. Mol. Microbiol. 9 (1993), 533–543.
38. Shapiro, J.A., Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52 (1998), 81–104.
39. Shioi, J.I., Imae, Y., Oosawa, F., Protonmotive force and motility of Bacillus subtilis. J. Bacteriol. 133 (1978), 1083–1088.
40. Shioi, J.I., Matsuura, S., Imae, Y., Quantitative measurements of proton motive force and motility in Bacillus subtilis. J. Bacteriol. 144 (1980), 891–897.
41. Trackpy Authors (2016). Trackpy. http://soft-matter.github.io/trackpy/v0.3.2/#.
42. Volfson, D., Cookson, S., Hasty, J., Tsimring, L.S., Biomechanical ordering of dense cell populations. Proc. Natl. Acad. Sci. USA 105 (2008), 15346–15351.
43. Waters, C.M., Bassler, B.L., Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21 (2005), 319–346.
44. Yasbin, R.E., Young, F.E., Transduction in Bacillus subtilis by bacteriophage SPP1. J. Virol. 14 (1974), 1343–1348.
45. Yi, T.-M., Huang, Y., Simon, M.I., Doyle, J., Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc. Natl. Acad. Sci. USA 97 (2000), 4649–4653.