Stochastic coordination of multiple actuators reduces latency and improves chemotactic response in bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 3, 2012, Pages 805-810

  Sneddona, Michael W ^a   Pontius, William ^a,b   Emonet, Thierry ^a,b  

^a YALE UNIVERSITY   (United States)

^b Yale University   (United States)

Author keywords

Agent based; L vy walk; Motility; Search strategy; Signal processing

Indexed keywords

CHEMOATTRACTANT; MOLECULAR MOTOR;

ARTICLE; BACTERIAL FLAGELLUM; CELL MOTION; CHEMOSENSITIVITY; CHEMOTAXIS; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; LATENT PERIOD; NONHUMAN; PRIORITY JOURNAL; SIGNAL DETECTION; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; STOCHASTIC MODEL;

CHEMOTAXIS; ESCHERICHIA COLI; FLAGELLA; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; MOLECULAR MOTOR PROTEINS; SIGNAL TRANSDUCTION; STOCHASTIC PROCESSES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84856402575     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1113706109     Document Type: Article

References (50)

1. Berg HC (2000) Motile behavior of bacteria. Phys Today 53:24-29.
2. Darnton NC, Turner L, Rojevsky S, Berg HC (2007) On torque and tumbling in swimming Escherichia coli. J Bacteriol 189:1756-1764. (Pubitemid 46446138)
3. Turner L, Ryu WS, Berg HC (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182:2793-2801. (Pubitemid 30246910)
4. Wadhams GH, Armitage JP (2004) Making sense of it all: Bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024-1037. (Pubitemid 39611538)
5. Block SM, Segall JE, Berg HC (1982) Impulse responses in bacterial chemotaxis. Cell 31:215-226. (Pubitemid 13215207)
6. Segall JE, Manson MD, Berg HC (1982) Signal processing times in bacterial chemotaxis. Nature 296:855-857. (Pubitemid 12096593)
7. Fahrner KA (1995) Studies of bacterial flagellar motors and filaments. PhD thesis (Harvard Univ Press, Cambridge, MA).
8. Cluzel P, Surette M, Leibler S (2000) An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287:1652-1655. (Pubitemid 30127766)
9. Sourjik V, Berg HC (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428:437-441. (Pubitemid 38419690)
10. Khan S, Jain S, Reid GP, Trentham DR (2004) The fast tumble signal in bacterial chemotaxis. Biophys J 86:4049-4058. (Pubitemid 38780280)
11. Korobkova E, Emonet T, Vilar JMG, Shimizu TS, Cluzel P (2004) From molecular noise to behavioural variability in a single bacterium. Nature 428:574-578. (Pubitemid 38480542)
12. Jasuja R, Keyoung J, Reid GP, Trentham DR, Khan S (1999) Chemotactic responses of Escherichia coli to small jumps of photoreleased L-aspartate. Biophys J 76:1706-1719. (Pubitemid 29262648)
13. Emonet T, Cluzel P (2008) Relationship between cellular response and behavioral variability in bacterial chemotaxis. Proc Natl Acad Sci USA 105:3304-3309. (Pubitemid 351723548)
14. Emonet T, Macal CM, North MJ, Wickersham CE, Cluzel P (2005) Agent Cell: A digital single-cell assay for bacterial chemotaxis. Bioinformatics 21:2714-2721. (Pubitemid 40852319)
15. Flores H, Lobaton E, Méndez-Diez S, Tlupova S, Cortez R (2005) A study of bacterial flagellar bundling. Bull Math Biol 67:137-168. (Pubitemid 40181072)
16. Kim M, Bird JC, Van Parys AJ, Breuer KS, Powers TR (2003) A macroscopic scale model of bacterial flagellar bundling. Proc Natl Acad Sci USA 100:15481-15485. (Pubitemid 38021015)
17. Lauga E, Powers TR (2009) The hydrodynamics of swimming microorganisms. Rep Prog Phys 72:096601.
18. Fahrner KA, Ryu WS, Berg HC (2003) Biomechanics: Bacterial flagellar switching under load. Nature 423:938. (Pubitemid 36806900)
19. Yuan J, Fahrner KA, Berg HC (2009) Switching of the bacterial flagellar motor near zero load. J Mol Biol 390:394-400.
20. Van Albada SB, Tǎ;nase-Nicola S, Ten Wolde PR (2009) The switching dynamics of the bacterial flagellar motor. Mol Syst Biol 5:316.
21. Tu Y (2008) The nonequilibrium mechanism for ultrasensitivity in a biological switch: Sensing by Maxwell's demons. Proc Natl Acad Sci USA 105:11737-11741.
22. Bai F, et al. (2010) Conformational spread as a mechanism for cooperativity in the bacterial flagellar switch. Science 327:685-689.
23. Sneddon MW, Faeder JR, Emonet T (2011) Efficient modeling, simulation and coarse-graining of biological complexity with NFsim. Nat Methods 8:177-183.
24. Tu Y, Grinstein G (2005) How white noise generates power-law switching in bacterial flagellar motors. Phys Rev Lett 94:208101.
25. Jiang L, Ouyang Q, Tu Y (2010) Quantitative modeling of Escherichia coli chemotactic motion in environments varying in space and time. PLoS Comput Biol 6:e1000735.
26. Vladimirov N, Løvdok L, Lebiedz D, Sourjik V (2008) Dependence of bacterial chemo-taxis on gradient shape and adaptation rate. PLoS Comput Biol 4:e1000242.
27. Matthäus F, Jagodic M, Dobnikar J (2009) E. coli superdiffusion and chemotaxis-search strategy, precision, and motility. Biophys J 97:946-957.
28. Kalinin YV, Jiang L, Tu Y, Wu M (2009) Logarithmic sensing in Escherichia coli bacterial chemotaxis. Biophys J 96:2439-2448.
29. Ishihara A, Segall JE, Block SM, Berg HC (1983) Coordination of flagella on filamentous cells of Escherichia coli. J Bacteriol 155:228-237. (Pubitemid 13071976)
30. Vladimirov N, Lebiedz D, Sourjik V (2010) Predicted auxiliary navigation mechanism of peritrichously flagellated chemotactic bacteria. PLoS Comput Biol 6:e1000717.
31. Park H, et al. (2010) Interdependence of behavioural variability and response to small stimuli in bacteria. Nature 468:819-823.
32. Mello BA, Tu Y (2005) An allosteric model for heterogeneous receptor complexes: Understanding bacterial chemotaxis responses to multiple stimuli. Proc Natl Acad Sci USA 102:17354-17359. (Pubitemid 41740870)
33. Endres RG, Wingreen NS (2006) Precise adaptation in bacterial chemotaxis through "assistance neighborhoods". Proc Natl Acad Sci USA 103:13040-13044. (Pubitemid 44338913)
34. Keymer JE, Endres RG, Skoge M, Meir Y, Wingreen NS (2006) Chemosensing in Escherichia coli: Two regimes of two-state receptors. Proc Natl Acad Sci USA 103:1786-1791. (Pubitemid 43228771)
35. Hansen CH, Endres RG, Wingreen NS (2008) Chemotaxis in Escherichia coli: A molecular model for robust precise adaptation. PLoS Comput Biol 4:e1.
36. Berg HC, Brown DA (1972) Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239:500-504.
37. Matthäus F, Mommer MS, Curk T, Dobnikar J (2011) On the origin and characteristics of noise-induced Lévy walks of E. coli. PLoS One 6:e18623.
38. Viswanathan GM, et al. (1999) Optimizing the success of random searches. Nature 401:911-914.
39. Edwards AM, et al. (2007) Revisiting Levy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449:1044-1048. (Pubitemid 350017586)
40. Gammaitoni L, Hänggi P, Jung P, Marchesoni F (1998) Stochastic resonance. Rev Mod Phys 70:223-223.
41. Duke TAJ, Le Novere N, Bray D (2001) Conformational spread in a ring of proteins: A stochastic approach to allostery1. J Mol Biol 308:541-553. (Pubitemid 33027618)
42. Meacci G, Lan G, Tu Y (2011) Dynamics of the bacterial flagellar motor: The effects of stator compliance, back steps, temperature, and rotational asymmetry. Biophys J 100:1986-1995.
43. Chen X, Berg HC (2000) Torque-speed relationship of the flagellar rotary motor of Escherichia coli. Biophys J 78:1036-1041. (Pubitemid 30211862)
44. Yuan J, Berg HC (2008) Resurrection of the flagellar rotary motor near zero load. Proc Natl Acad Sci USA 105:1182-1185. (Pubitemid 351397027)
45. Yuan J, Fahrner KA, Turner L, Berg HC (2010) Asymmetry in the clockwise and counter-clockwise rotation of the bacterial flagellar motor. Proc Natl Acad Sci USA 107:12846-12849.
46. Cai L, Dalal CK, Elowitz MB (2008) Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 455:485-490.
47. Eldar A, Elowitz MB (2010) Functional roles for noise in genetic circuits. Nature 467:167-173.
48. Monod J, Wyman J, Changeux J-P (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12:88-118.
49. Gillespie DT (1996) The mathematics of Brownian motion and Johnson noise. Am J Phys 64:225-240.
50. Berg HC (1993) Random Walks in Biology (Princeton Univ Press, Princeton, NJ).