The physical and functional thermal sensitivity of bacterial chemoreceptors

Journal of Molecular Biology

Volumn 411, Issue 3, 2011, Pages 554-566

  Frank, Vered ^a   Koler, Moriah ^a   Furst, Smadar ^a   Vaknin, Ady ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

bacterial chemotaxis; fluorescence polarization; FRET; receptor clustering; thermal sensitivity

Indexed keywords

DIMER; MEMBRANE RECEPTOR; PHOSPHOTRANSFERASE;

ARTICLE; CHEMORECEPTOR; CHEMOTAXIS; CROSS LINKING; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEAT SENSITIVITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79960911333     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.06.006     Document Type: Article

References (59)

1. Kirby J.R. Chemotaxis-like regulatory systems: unique roles in diverse bacteria Annu. Rev. Microbiol. 63 2009 45 59
2. Hazelbauer G.L., Falke J.J., and Parkinson J.S. Bacterial chemoreceptors: high-performance signaling in networked arrays Trends Biochem. Sci. 33 2008 9 19
3. Baker M.D., Wolanin P.M., and Stock J.B. Systems biology of bacterial chemotaxis Curr. Opin. Microbiol. 9 2006 187 192
4. Berg H.C. E. coli in Motion 2004 Springer New York, NY
5. Parkinson J.S. Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases Annu. Rev. Microbiol. 64 2010 101 122
6. Maddock J.R., and Shapiro L. Polar location of the chemoreceptor complex in the Escherichia coli cell Science 259 1993 1717 1723 (Pubitemid 23114656)
7. Sourjik V., and Berg H.C. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions Mol. Microbiol. 37 2000 740 751 (Pubitemid 30618137)
8. Kim K.K., Yokota H., and Kim S.H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor Nature 400 1999 787 792 (Pubitemid 29399543)
9. Shimizu T.S., Le Novere N., Levin M.D., Beavil A.J., Sutton B.J., and Bray D. Molecular model of a lattice of signalling proteins involved in bacterial chemotaxis Nat. Cell Biol. 2 2000 792 796
10. Parkinson J.S., Ames P., and Studdert C.A. Collaborative signaling by bacterial chemoreceptors Curr. Opin. Microbiol. 8 2005 116 121 (Pubitemid 40417950)
11. Zhang P., Khursigara C.M., Hartnell L.M., and Subramaniam S. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy Proc. Natl Acad. Sci. USA 104 2007 3777 3781 (Pubitemid 47181530)
12. Khursigara C.M., Wu X., Zhang P., Lefman J., and Subramaniam S. Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors Proc. Natl Acad. Sci. USA 105 2008 16555 16560
13. Duke T.A.J., and Bray D. Heightened sensitivity of a lattice of membrane receptors Proc. Natl Acad. Sci. USA 96 1999 10104 10108 (Pubitemid 29422519)
14. Bray D., Levin M.D., and Morton-Firth C.J. Receptor clustering as a cellular mechanism to control sensitivity Nature 393 1998 85 88 (Pubitemid 28240260)
15. Gestwicki J.E., and Kiessling L.L. Inter-receptor communication through arrays of bacterial chemoreceptors Nature 415 2002 81 84 (Pubitemid 34062453)
16. Lai R.Z., Manson J.M.B., Bormans A.F., Draheim R.R., Nguyen N.T., and Manson M.D. Cooperative signaling among bacterial chemoreceptors Biochemistry 44 2005 14298 14307 (Pubitemid 41533054)
17. Li G., and Weis R.M. Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli Cell 100 2000 357 365 (Pubitemid 30353091)
18. Sourjik V., and Berg H.C. Functional interactions between receptors in bacterial chemotaxis Nature 428 2004 437 441 (Pubitemid 38419690)
19. Mello B.A., and Tu Y. An allosteric model for heterogeneous receptor complexes: understanding bacterial chemotaxis responses to multiple stimuli Proc. Natl Acad. Sci. USA 102 2005 17354 17359 (Pubitemid 41740870)
20. Keymer J.E., Endres R.G., Skoge M., Meir Y., and Wingreen N.S. Chemosensing in Escherichia coli: two regimes of two-state receptors Proc. Natl Acad. Sci. USA 103 2006 1786 1791 (Pubitemid 43228771)
21. Briegel A., Ortega D.R., Tocheva E.I., Wuichet K., Li Z., and Chen S. Universal architecture of bacterial chemoreceptor arrays Proc. Natl Acad. Sci. USA 106 2009 17181 17186
22. Ariane B., Ding H.J., Zhuo L., John W., Zemer G., and Dias D.P. Location and architecture of the Caulobacter crescentus chemoreceptor array Mol. Microbiol. 69 2008 30 41 (Pubitemid 351832749)
23. Park S.Y., Borbat P.P., Gonzalez-Bonet G., Bhatnagar J., Pollard A.M., and Freed J.H. Reconstruction of the chemotaxis receptor-kinase assembly Nat. Struct. Mol. Biol. 13 2006 400 407 (Pubitemid 43881579)
24. Maeda K., and Imae Y. Thermosensory transduction in Escherichia coli: inhibition of the thermoresponse by l-serine Proc. Natl Acad. Sci. USA 76 1979 91 95 (Pubitemid 9081732)
25. Maeda K., Imae Y., Shioi J.I., and Oosawa F. Effect of temperature on motility and chemotaxis of Escherichia coli J. Bacteriol. 127 1976 1039 1046
26. Nara T., Kawagishi I., Nishiyama S. i., Homma M., and Imae Y. Modulation of the thermosensing profile of the Escherichia coli aspartate receptor Tar by covalent modification of its methyl-accepting sites J. Biol. Chem. 271 1996 17932 17936 (Pubitemid 26250774)
27. Nishiyama S.I., Ohno S., Ohta N., Inoue Y., Fukuoka H., Ishijima A., and Kawagishi I. Thermosensing function of the Escherichia coli redox sensor Aer J. Bacteriol. 192 2010 1740 1743
28. Paster E., and Ryu W.S. The thermal impulse response of Escherichia coli Proc. Natl Acad. Sci. USA 105 2008 5373 5377 (Pubitemid 351753870)
29. 13DK106YW Biophys. J. 77 1999 597 603 (Pubitemid 29305255)
30. Yuan J., and Berg H.C. Thermal and solvent-isotope effects on the flagellar rotary motor near zero load Biophys. J. 98 2010 2121 2126
31. Wu J., Long D.G., and Weis R.M. Reversible dissociation and unfolding of the Escherichia coli aspartate receptor cytoplasmic fragment Biochemistry 34 1995 3056 3065
32. Erbse A.H., and Falke J.J. The core signaling proteins of bacterial chemotaxis assemble to form an ultrastable complex Biochemistry 48 2009 6975 6987
33. Adler J. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli J. Gen. Microbiol. 74 1973 77 91
34. Vaknin A., and Berg H.C. Osmotic stress mechanically perturbs chemoreceptors in Escherichia coli Proc. Natl Acad. Sci. USA 103 2006 592 596 (Pubitemid 43153070)
35. Vaknin A., and Berg H.C. Physical responses of bacterial chemoreceptors J. Mol. Biol. 366 2007 1416 1423 (Pubitemid 46215608)
36. Sourjik, V., Vaknin, A., Shimizu, T. S. & Berg, H. C. (2007). In vivo measurement by FRET of pathway activity in bacterial chemotaxis. In Methods in Enzymology (Simon, M. I., Crane, B. R. & Alexandrine, C., eds.), vol. 423, pp. 363, 365-391. Academic Press New York, NY.
37. Cantwell B.J., Draheim R.R., Weart R.B., Nguyen C., Stewart R.C., and Manson M.D. CheZ phosphatase localizes to chemoreceptor patches via CheA-short J. Bacteriol. 185 2003 2354 2361 (Pubitemid 36363197)
38. Vaknin A., and Berg H.C. Single-cell FRET imaging of phosphatase activity in the Escherichia coli chemotaxis system Proc. Natl. Acad. Sci. USA 101 2004 17072 17077 (Pubitemid 39627776)
39. Mowbray S.L., and Koshland D.E. Mutations in the aspartate receptor of Escherichia coli which affect aspartate binding J. Biol. Chem. 265 1990 15638 15643
40. Gardina P., Conway C., Kossman M., and Manson M. Aspartate and maltose-binding protein interact with adjacent sites in the Tar chemotactic signal transducer of Escherichia coli J. Bacteriol. 174 1992 1528 1536
41. Antommattei F.M., Munzner J.B., and Weis R.M. Ligand-specific activation of Escherichia coli chemoreceptor transmethylation J. Bacteriol. 186 2004 7556 7563 (Pubitemid 39463719)
42. Vaknin A., and Berg H.C. Direct evidence for coupling between bacterial chemoreceptors J. Mol. Biol. 382 2008 573 577
43. Studdert C.A., and Parkinson J.S. Crosslinking snapshots of bacterial chemoreceptor squads Proc. Natl Acad. Sci. USA 101 2004 2117 2122 (Pubitemid 38229024)
44. Studdert C.A., and Parkinson J.S. Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies Proc. Natl Acad. Sci. USA 102 2005 15623 15628 (Pubitemid 41528106)
45. Park C., Dutton D.P., and Hazelbauer G.L. Effects of glutamines and glutamates at sites of covalent modification of a methyl-accepting transducer J. Bacteriol. 172 1990 7179 7187
46. Dunten P., and Koshland D.E. Tuning the responsiveness of a sensory receptor via covalent modification J. Biol. Chem. 266 1991 1491 1496 (Pubitemid 21908329)
47. Bornhorst J.A., and Falke J.J. Evidence that both ligand binding and covalent adaptation drive a two-state equilibrium in the aspartate receptor signaling complex J. Gen. Physiol. 118 2001 693 710 (Pubitemid 33131101)
48. Sourjik V., and Berg H.C. Receptor sensitivity in bacterial chemotaxis Proc. Natl Acad. Sci. USA 99 2002 123 127 (Pubitemid 34060327)
49. Greenfield D., McEvoy A.L., Shroff H., Crooks G.E., Wingreen N.S., Betzig E., and Liphardt J. Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy PLoS Biol. 7 2009 e1000137
50. Oleksiuk O., Jakovljevic V., Vladimirov N., Carvalho R., Paster E., and Ryu W.S. Thermal robustness of signaling in bacterial chemotaxis Cell 145 2011 312 321
51. Zhou Q., Ames P., and Parkinson J.S. Mutational analyses of HAMP helices suggest a dynamic bundle model of input-output signalling in chemoreceptors Mol. Microbiol. 73 2009 801 814
52. Swain K.E., Gonzalez M.A., and Falke J.J. Engineered socket study of signaling through a four-helix bundle: evidence for a Yin-Yang mechanism in the kinase control module of the aspartate receptor Biochemistry 48 2009 9266 9277
53. Alexander R.P., and Zhulin I.B. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors Proc. Natl Acad. Sci. USA 104 2007 2885 2890 (Pubitemid 46327974)
54. Kim S.H., Wang W., and Kim K.K. Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity Proc. Natl Acad. Sci. USA 99 2002 11611 11615 (Pubitemid 34994447)
55. Salman H., Zilman A., Loverdo C., Jeffroy M., and Libchaber A. Solitary modes of bacterial culture in a temperature gradient Phys. Rev. Lett. 97 2006 118101
56. Nara T., Lee L., and Imae Y. Thermosensing ability of Trg and Tap chemoreceptors in Escherichia coli J. Bacteriol. 173 1991 1120 1124
57. Shimizu T.S., Tu Y., and Berg H.C. A modular gradient-sensing network for chemotaxis in Escherichia coli revealed by responses to time-varying stimuli Mol. Syst. Biol. 6 2010 382
58. Yuan J., and Berg H.C. Thermal and solvent-isotope effects on the flagellar rotary motor near zero load Biophys. J. 98 2010 2121 2126
59. Parkinson J.S., and Houts S.E. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions J. Bacteriol. 151 1982 106 113 (Pubitemid 12022312)