Bacterial chemotaxis: Information processing, thermodynamics, and behavior

Current Opinion in Microbiology

Volumn 30, Issue , 2016, Pages 8-15

  Micali, Gabriele ^a   Endres, Robert G ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CHEA KINASE; CHEW PROTEIN;

ADAPTATION; BACTERIAL CELL; BACTERIAL CHEMOTAXIS; BACTERIAL PHENOMENA AND FUNCTIONS; CELL FUNCTION; CHEMOTAXIS; ENVIRONMENTAL FACTOR; ESCHERICHIA COLI; INFORMATION PROCESSING; INFORMATION SCIENCE; LIGAND BINDING; NONHUMAN; NUTRIENT; REVIEW; THERMODYNAMICS; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CHEMOTAXIS; ESCHERICHIA COLI; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; THERMODYNAMICS;

EID: 84951325747     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2015.12.001     Document Type: Review

References (63)

1. Parkinson J.S., Hazelbauer G.L., Falke J.J. Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Trends Microbiol 2015, 23:257-266.
2. Tu Y. Quantitative modeling of bacterial chemotaxis: signal amplification and accurate adaptation. Annu Rev Biophys 2013, 42:337-359.
3. Sourjik V., Wingreen N.S. Responding to chemical gradients: bacterial chemotaxis. Curr Opin Cell Biol 2012, 24:262-268.
4. Jones C.W., Armitage J.P. Positioning of bacterial chemoreceptors. Trends Microbiol 2015, 23:247-256.
5. Bi S., Lai L. Bacterial chemoreceptors and chemoeffectors. Cell Mol Life Sci 2014, 72:691-708.
6. Nataro J., Cohen P., Mobley H.W.J. Colonization of Mucosal Surfaces 2005, ASM Press.
7. Darnton N.C., Turner L., Rojevsky S., Berg H.C. On torque and tumbling in swimming Escherichia coli. J Bacteriol 2007, 189:1756-1764.
8. Turner L., Ryu W.S., Berg H.C. Real-time imaging of fluorescent flagellar filaments. J Bacteriol 2000, 182:2793-2801.
9. Saragosti J., Calvez V., Bournaveas N., Perthame B., Buguin A., Silberzan P. Directional persistence of chemotactic bacteria in a traveling concentration wave. Proc Natl Acad Sci U S A 2011, 108:16235-16240.
10. Berg H.C., Purcell E.M. Physics of chemoreception. Biophys J 1977, 20:193-219.
11. Endres R.G., Wingreen N.S. Maximum likelihood and the single receptor. Phys Rev Lett 2009, 103:1-4.
12. Mao H., Cremer P.S., Manson M.D. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc Natl Acad Sci U S A 2003, 100:5449-5454.
13. Berg H.C., Tedesco P.M. Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci U S A 1975, 72:3235-3239.
14. Mesibov R., Ordal G.W., Adler J. The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range. Weber law and related phenomena. J Gen Physiol 1973, 62:203-223.
15. Duke T.A.J., Bray D. Heightened sensitivity of a lattice of membrane receptors. Proc Natl Acad Sci U S A 1999, 96:10104-10108.
16. Sourjik V., Berg H.C. Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci U S A 2002, 99:123-127.
17. Keymer J.E., Endres R.G., Skoge M., Meir Y., Wingreen N.S. Chemosensing in Escherichia coli: two regimes of two-state receptors. Proc Natl Acad Sci U S A 2006, 103:1786-1791.
18. Endres R.G., Wingreen N.S. Precise adaptation in bacterial chemotaxis through "assistance neighborhoods". Proc Natl Acad Sci U S A 2006, 103:13040-13044.
19. Barkai N., Leibler S. Robustness in simple biochemical networks to transfer and process information. Nature 1997, 387:913-917.
20. Masson J.-B., Voisinne G., Wong-Ng J., Celani A., Vergassola M. Noninvasive inference of the molecular chemotactic response using bacterial trajectories. Proc Natl Acad Sci U S A 2012, 109:1802-1807.
21. Min T.L., Mears P.J., Golding I., Chemla Y.R. Chemotactic adaptation kinetics of individual Escherichia coli cells. Proc Natl Acad Sci U S A 2012, 109:9869-9874.
22. Neumann S., Vladimirov N., Krembel A.K., Wingreen N.S., Sourjik V. Imprecision of adaptation in Escherichia coli chemotaxis. PLoS One 2014, 9:1-6.
23. Shoval O., Goentoro L., Hart Y., Mayo A., Sontag E., Alon U. Fold-change detection and scalar symmetry of sensory input fields. Proc Natl Acad Sci U S A 2010, 107:15995-16000.
24. Krembel A.K., Neumann S., Sourjik V. Universal response-adaptation relation in bacterial chemotaxis. J Bacteriol 2015, 197:307-313.
25. Kalinin Y.V., Jiang L., Tu Y., Wu M. Logarithmic sensing in Escherichia coli bacterial chemotaxis. Biophys J 2009, 96:2439-2448.
26. Oleksiuk O., Jakovljevic V., Vladimirov N., Carvalho R., Paster E., Ryu W.S., Meir Y., Wingreen N.S., Kollmann M., Sourjik V. Thermal robustness of signaling in bacterial chemotaxis. Cell 2011, 145:312-321.
27. Yang Y., Sourjik V. Opposite responses by different chemoreceptors set a tunable preference point in Escherichia coli pH taxis. Mol Microbiol 2012, 86:1482-1489.
28. Clausznitzer D., Micali G., Neumann S., Sourjik V., Endres R.G. Predicting chemical environments of bacteria from receptor signaling. PLoS Comput Biol 2014, 10:e1003870.
29. Cluzel P., Surette M., Leibler S. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 2000, 287:1652-1655.
30. Yuan J., Berg H.C. Ultrasensitivity of an adaptive bacterial motor. J Mol Biol 2013, 425:1760-1764.
31. Dufour Y.S., Fu X., Hernandez-Nunez L., Emonet T. Limits of feedback control in bacterial chemotaxis. PLoS Comput Biol 2014, 10:e1003694.
32. Tostevin F., Ten Wolde P.R. Mutual information between input and output trajectories of biochemical networks. Phys Rev Lett 2009, 102:1-4.
33. Hoh J.H., Heinz W.F., Werbin J.L. Spatial information analysis of chemotactic trajectories. J Biol Phys 2012, 38:365-381.
34. Laughlin S.B., Steveninck R.R.D.R.Van, Anderson J.C. The metabolic cost of neural information. Nat Neurosci 1998, 1:36-41.
35. Laughlin S.B. A simple coding procedure enhances a neuron's information capacity. Z Naturforsch C 1981, 36:910-912.
36. Laughlin S.B. Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 2001, 11:475-480.
37. Bérut A., Arakelyan A., Petrosyan A., Ciliberto S., Dillenschneider R., Lutz E. Experimental verification of Landauer's principle linking information and thermodynamics. Nature 2012, 483:187-189.
38. Mehta P., Schwab D.J. Energetic costs of cellular computation. Proc Natl Acad Sci U S A 2012, 109:17978-17982.
39. Govern C.C., ten Wolde P.R. Optimal resource allocation in cellular sensing systems. Proc Natl Acad Sci U S A 2014, 111:17486-17491.
40. Barato A.C., Hartich D., Seifert U. Efficiency of cellular information processing. New J Phys 2014, 16:103024.
41. Sartori P., Granger L., Lee C., Horowitz J. Thermodynamic costs of information processing in sensory adaption. PLoS Comput Biol 2014, 10:e1003974.
42. De Palo G., Endres R.G. Unraveling adaptation in eukaryotic pathways: lessons from protocells. PLoS Comput Biol 2013, 9:e1003300.
43. Lan G., Sartori P., Neumann S., Sourjik V., Tu Y. The energy-speed-accuracy trade-off in sensory adaptation. Nat Phys 2012, 8:422-428.
44. Govern C.C., ten Wolde R.P. Energy dissipation and noise correlations in biochemical sensing. Phys Rev Lett 2014, 113:1-5.
45. Sartori P., Tu Y. Free energy cost of reducing noise while maintaining a high sensitivity. Phys Rev Lett 2015, 118102:1-5.
46. Li M., Hazelbauer G.L. Cellular stoichiometry of the components of the chemotaxis signaling complex. J Bacteriol 2004, 186:3687-3694.
47. Vladimirov N., Løvdok L., Lebiedz D., Sourjik V. Dependence of bacterial chemotaxis on gradient shape and adaptation rate. PLoS Comput Biol 2008, 4:e1000242.
48. Alon U., Surette M.G., Barkai N., Leibler S. Robustness in bacterial chemotaxis. Nature 1999, 397:168-171.
49. Thiem S., Sourjik V. Stochastic assembly of chemoreceptor clusters in Escherichia coli. Mol Microbiol 2008, 68:1228-1236.
50. Cohen-ben-lulu G.N., Francis N.R., Shimoni E., Noy D., Davidov Y., Prasad K., Sagi Y., Cecchini G., Johnstone R.M., Eisenbach M. The bacterial flagellar switch complex is getting more complex. EMBO J 2008, 27:1134-1144.
51. Frankel N.W., Pontius W., Dufour Y.S., Long J., Hernandez-Nunez L., Emonet T. Adaptability of non-genetic diversity in bacterial chemotaxis. Elife 2014, 3:1-30.
52. Yuan J., Branch R.W., Hosu B.G., Berg H.C. Adaptation at the output of the chemotaxis signalling pathway. Nature 2012, 484:233-236.
53. Lele P.P., Branch R.W., Nathan V.S.J., Berg H.C. Mechanism for adaptive remodeling of the bacterial flagellar switch. Proc Natl Acad Sci U S A 2012, 109:20018-20022.
54. Min T.L., Mears P.J., Chubiz L.M., Rao C.V., Golding I., Chemla Y.R. Bacterial motility using optical tweezers. Nat Methods 2009, 6:831-835.
55. Mears P.J., Koirala S., Rao C.V., Golding I., Chemla Y.R. Escherichia coli swimming is robust against variations in flagellar number. Elife 2014, 2014:1-18.
56. Sneddon M.W., Pontius W., Emonet T. Stochastic coordination of multiple actuators reduces latency and improves chemotactic response in bacteria. Proc Natl Acad Sci 2012, 109:805-810.
57. Hu B., Tu Y. Coordinated switching of bacterial flagellar motors: evidence for direct motor-motor coupling?. Phys Rev Lett 2013, 110:1-5.
58. Shannon C.E. A mathematical theory of communication. Bell Syst Tech J 1948, 27:379-423.
59. Mahon S.S.M., Sim A., Filippi S., Johnson R., Liepe J., Smith D., Stumpf M.P.H. Information theory and signal transduction systems: from molecular information processing to network inference. Semin Cell Dev Biol 2014, 35:1-11.
60. Kraskov A., Stögbauer H., Grassberger P. Estimating mutual information. Phys Rev E - Stat Nonlinear Soft Matter Phys 2004, 69:1-16.
61. Bowsher C.G., Swain P.S. Environmental sensing, information transfer, and cellular decision-making. Curr Opin Biotechnol 2014, 28:149-155.
62. Tkacik G., Callan C.G., Bialek W. Information flow and optimization in transcriptional regulation. Proc Natl Acad Sci U S A 2008, 105:12265-12270.
63. Parrondo J.M.R., Horowitz J.M., Sagawa T. Thermodynamics of information. Nat Phys 2015, 11:131-139.