Phenol sensing by Escherichia coli chemoreceptors: A nonclassical mechanism

Journal of Bacteriology

Volumn 193, Issue 23, 2011, Pages 6597-6604

  Pham, Hai The ^a,b   Parkinson, John S ^a  

^a UNIVERSITY OF UTAH   (United States)

^b VIETNAM NATIONAL UNIVERSITY   (Viet Nam)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROL; PHENOL; BACTERIAL PROTEIN; CELL SURFACE RECEPTOR; ESCHERICHIA COLI PROTEIN; MEMBRANE PROTEIN; METHYL ACCEPTING CHEMOTAXIS PROTEINS; METHYL-ACCEPTING CHEMOTAXIS PROTEINS; TAR PROTEIN, E COLI;

ARTICLE; CELL MEMBRANE; CELL PH; CELL STRUCTURE; CHEMORECEPTOR; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; HELIX (SNAIL); METHYLATION; MOLECULE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TAP CHEMORECEPTOR; TAR CHEMORECEPTOR; TEMPERATURE; TRG CHEMORECEPTOR; TSR CHEMORECEPTOR; CHEMISTRY; CHEMOTAXIS; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ESCHERICHIA COLI; PSEUDOMONAS;

BACTERIAL PROTEINS; CHEMOTAXIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PHENOL; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE;

EID: 84855403705     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05987-11     Document Type: Article

References (61)

1. Adler, J. 1973. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J. Gen. Microbiol. 74:77-91.
2. Airola, M., K. J. Watts, and B. R. Crane. 2010. Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure 18:436-448.
3. Alexander, R. P., and I. B. Zhulin. 2007. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc. Natl. Acad. Sci. U. S. A. 104:2885-2890.
4. Ames, P., and J. S. Parkinson. 1994. Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor. J. Bacteriol. 176:6340-6348.
5. Ames, P., C. A. Studdert, R. H. Reiser, and J. S. Parkinson. 2002. Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99:7060-7065.
6. Ames, P., Y. A. Yu, and J. S. Parkinson. 1996. Methylation segments are not required for chemotactic signalling by cytoplasmic fragments of Tsr, the methyl-accepting serine chemoreceptor of Escherichia coli. Mol. Microbiol. 19:737-746.
7. Bibikov, S. I., A. C. Miller, K. K. Gosink, and J. S. Parkinson. 2004. Methylation-independent aerotaxis mediated by the Escherichia coli Aer protein. J. Bacteriol. 186:3730-3737.
8. Björkman, A. M., P. Dunten, M. O. Sandgren, V. N. Dwarakanath, and S. L. Mowbray. 2001. Mutations that affect ligand binding to the Escherichia coli aspartate receptor: implications for transmembrane signaling. J. Biol. Chem. 276:2808-2815.
9. Bolivar, F., et al. 1977. Construction and characterization of new cloning vehicles. Gene 2:95-113.
10. Brown, D. A., and H. C. Berg. 1974. Temporal stimulation of chemotaxis in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 71:1388-1392.
11. Burón-Barral, M., K. K. Gosink, and J. S. Parkinson. 2006. Loss- and gain-of-function mutations in the F1-HAMP region of the Escherichia coli aerotaxis transducer Aer. J. Bacteriol. 188:3477-3486.
12. Chang, A. C. Y., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the p15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
13. Dunin-Horkawicz, S., and A. N. Lupas. 2010. Comprehensive analysis of HAMP domains: implications for transmembrane signal transduction. J. Mol. Biol. 397:1156-1174.
14. Fleeger, J. W., K. R. Carman, and R. M. Nisbet. 2003. Indirect effects of contaminants in aquatic ecosystems. Sci. Total Environ. 317:207-233.
15. Gosink, K. K., M. Buron-Barral, and J. S. Parkinson. 2006. Signaling interactions between the aerotaxis transducer Aer and heterologous chemoreceptors in Escherichia coli. J. Bacteriol. 188:3487-3493.
16. Harayama, S., E. T. Palva, and G. L. Hazelbauer. 1979. Transposon-insertion mutants of Escherichia coli K12 defective in a component common to galactose and ribose chemotaxis. Mol. Gen. Genet. 171:193-203.
17. Hazelbauer, G. L. 1975. Maltose chemoreceptor of Escherichia coli. J. Bacteriol. 122:206-214.
18. Hazelbauer, G. L., J. J. Falke, and J. S. Parkinson. 2008. Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem. Sci. 33:9-19.
19. Hegde, M., et al. 2011. Chemotaxis to the quorum-sensing signal AI-2 requires the Tsr chemoreceptor and the periplasmic LsrB AI-2-binding protein. J. Bacteriol. 193:768-773.
20. Hulko, M., et al. 2006. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929-940.
21. Imae, Y., K. Oosawa, T. Mizuno, M. Kihara, and R. M. Macnab. 1987. Phenol: a complex chemoeffector in bacterial chemotaxis. J. Bacteriol. 169:371-379.
22. Kihara, M., and R. M. Macnab. 1981. Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. J. Bacteriol. 145:1209-1221.
23. Kim, K. K., H. Yokota, and S. H. Kim. 1999. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400:787-792.
24. Kitanovic, S., P. Ames, and J. S. Parkinson. 2011. Mutational analysis of the control cable that mediates transmembrane signaling in the E. coli serine chemoreceptor. J. Bacteriol. 193:5062-5072.
25. Krikos, A., M. P. Conley, A. Boyd, H. C. Berg, and M. I. Simon. 1985. Chimeric chemosensory transducers of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 82:1326-1330.
26. Lai, W. C., B. D. Beel, and G. L. Hazelbauer. 2006. Adaptational modification and ligand occupancy have opposite effects on positioning of the transmembrane signalling helix of a chemoreceptor. Mol. Microbiol. 61:1081-1090.
27. Liu, J. D., and J. S. Parkinson. 1991. Genetic evidence for interaction between the CheW and Tsr proteins during chemoreceptor signaling by Escherichia coli. J. Bacteriol. 173:4941-4951.
28. Liu, X., and R. E. Parales. 2008. Chemotaxis of Escherichia coli to pyrimidines: a new role for the signal transducer Tap. J. Bacteriol. 190:972-979.
29. Macnab, R. M., and D. E. Koshland, Jr. 1972. The gradient-sensing mechanism in bacterial chemotaxis. Proc. Natl. Acad. Sci. U. S. A. 69:2509-2512.
30. Maeda, K., Y. Imae, J. I. Shioi, and F. Oosawa. 1976. Effect of temperature on motility and chemotaxis of Escherichia coli. J. Bacteriol. 127:1039-1046.
31. Manson, M. D., V. Blank, G. Brade, and C. F. Higgins. 1986. Peptide chemotaxis in E. coli involves the Tap signal transducer and the dipeptide permease. Nature 321:253-256.
32. Milburn, M. V., et al. 1991. Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science 254:1342-1347.
33. Mukherjee, S., S. Kumar, A. K. Misra, and M. Fan. 2007. Removal of phenols from water environment by activated carbon, bagasse ash and wood charcoal. Chem. Eng. J. 129:133-142.
34. Nara, T., I. Kawagishi, S. Nishiyama, M. Homma, and Y. Imae. 1996. Modulation of the thermosensing profile of the Escherichia coli aspartate receptor Tar by covalent modification of its methyl-accepting sites. J. Biol. Chem. 271:17932-17936.
35. Nishiyama, S., I. N. Maruyama, M. Homma, and I. Kawagishi. 1999. Inversion of thermosensing property of the bacterial receptor Tar by mutations in the second transmembrane region. J. Mol. Biol. 286:1275-1284.
36. Nishiyama, S., T. Nara, M. Homma, Y. Imae, and I. Kawagishi. 1997. Thermosensing properties of mutant aspartate chemoreceptors with methylaccepting sites replaced singly or multiply by alanine. J. Bacteriol. 179:6573-6580.
37. Nishiyama, S., et al. 2010. Thermosensing function of the Escherichia coli redox sensor Aer. J. Bacteriol. 192:1740-1743.
38. Nunes, C., et al. 2008. Substituted phenols as pollutants that affect membrane fluidity. J. Environ. Biol. 29:733-738.
39. Oosawa, K., and Y. Imae. 1983. Glycerol and ethylene glycol: members of a new class of repellents of Escherichia coli chemotaxis. J. Bacteriol. 154:104-112.
40. Pandey, G., and R. K. Jain. 2002. Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl. Environ. Microbiol. 68:5789-5795.
41. Parkinson, J. S. 1976. cheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J. Bacteriol. 126:758-770.
42. Parkinson, J. S. 2010. Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu. Rev. Microbiol. 64:101-122.
43. Repaske, D. R., and J. Adler. 1981. Change in intracellular pH of Escherichia coli mediates the chemotactic response to certain attractants and repellents. J. Bacteriol. 145:1196-1208.
44. Segall, J. E., S. M. Block, and H. C. Berg. 1986. Temporal comparisons in bacterial chemotaxis. Proc. Natl. Acad. Sci. U. S. A. 83:8987-8991.
45. Sikkema, J., J. A. de Bont, and B. Poolman. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59:201-222.
46. Sinha, J., S. J. Reyes, and J. P. Gallivan. 2010. Reprogramming bacteria to seek and destroy an herbicide. Nat. Chem. Biol. 6:464-470.
47. Springer, M. S., M. F. Goy, and J. Adler. 1977. Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc. Natl. Acad. Sci. U. S. A. 74:3312-3316.
48. Springer, W. R., and D. E. Koshland, Jr. 1977. Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc. Natl. Acad. Sci. U. S. A. 74:533-537.
49. Stock, J. B., and D. E. Koshland, Jr. 1978. A protein methylesterase involved in bacterial sensing. Proc. Natl. Acad. Sci. U. S. A. 75:3659-3663.
50. Studdert, C. A., and J. S. Parkinson. 2004. Crosslinking snapshots of bacterial chemoreceptor squads. Proc. Natl. Acad. Sci. U. S. A. 101:2117-2122.
51. Studdert, C. A., and J. S. Parkinson. 2005. Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc. Natl. Acad. Sci. U. S. A. 102:15623-15628.
52. Swain, K. E., M. A. Gonzalez, and J. J. Falke. 2009. 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 48:9266-9277.
53. Umemura, T., Y. Matsumoto, K. Ohnishi, M. Homma, and I. Kawagishi. 2002. Sensing of cytoplasmic pH by bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices. J. Biol. Chem. 277:1593-1598.
54. Wolfe, A. J., and H. C. Berg. 1989. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. U. S. A. 86:6973-6977.
55. Wolff, C., and J. S. Parkinson. 1988. Aspartate taxis mutants of the Escherichia coli Tar chemoreceptor. J. Bacteriol. 170:4509-4515.
56. Yamamoto, K., R. M. Macnab, and Y. Imae. 1990. Repellent response functions of the Trg and Tap chemoreceptors of Escherichia coli. J. Bacteriol. 172:383-388.
57. Yen, K. M. 1991. Construction of cloning cartridges for development of expression vectors in Gram-negative bacteria. J. Bacteriol. 173:5328-5335.
58. Zhao, J., and J. S. Parkinson. 2006. Mutational analysis of the chemoreceptor-coupling domain of the Escherichia coli chemotaxis signaling kinase CheA. J. Bacteriol. 188:3299-3307.
59. Zhou, Q., P. Ames, and J. S. Parkinson. 2011. Biphasic control logic of HAMP domain signalling in the Escherichia coli serine chemoreceptor. Mol. Microbiol. 80:596-611.
60. Zhou, Q., P. Ames, and J. S. Parkinson. 2009. Mutational analyses of HAMP helices suggest a dynamic bundle model of input-output signalling in chemoreceptors. Mol. Microbiol. 73:801-814.
61. Zhulin, I. B. 2001. The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv. Microb. Physiol. 45:157-198.