Interactions among the three adaptation systems of Bacillus subtilis chemotaxis as revealed by an in vitro receptor-kinase assay

Molecular Microbiology

Volumn 93, Issue 6, 2014, Pages 1104-1118

  Walukiewicz, Hanna E ^a,b   Tohidifar, Payman ^a   Ordal, George W ^b   Rao, Christopher V ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; BACTERIAL PROTEIN; CHEA HISTIDINE KINASE; CHEW PROTEIN; GLUTAMIC ACID; PHOSPHATASE; PHOSPHORYLATED PROTEIN CHEY; PROTEIN CHEC; PROTEIN CHED; PROTEIN CHEV; PROTEIN HISTIDINE KINASE; PROTEIN MCPB; RECEPTOR; UNCLASSIFIED DRUG; CHED PROTEIN, BACILLUS SUBTILIS; CHEMOTACTIC FACTOR; CHEV PROTEIN, BACTERIA; PROTEIN BINDING; PROTEIN KINASE;

ADAPTATION; AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL PHENOMENA AND FUNCTIONS; BINDING AFFINITY; BIOASSAY; CHEC CHED CHEYP ADAPTATION SYSTEM; CHEMOTAXIS; CHEV ADAPTATION SYSTEM; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; METHYLATION ADAPTATION SYSTEM; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RECEPTOR KINASE ASSAY; SENSORY ADAPTATION; SIGNAL TRANSDUCTION; STOICHIOMETRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; METHYLATION; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHEMOTACTIC FACTORS; CHEMOTAXIS; GENE EXPRESSION REGULATION, BACTERIAL; METHYLATION; PROTEIN BINDING; PROTEIN KINASES;

EID: 84908548325     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12721     Document Type: Article

References (50)

1. Adler, J. (1966) Chemotaxis in bacteria. Science 153: 708-716.
2. Berg, H.C., and Purcell, E.M. (1977) Physics of chemoreception. Biophys J 20: 193-219.
3. Bischoff, D.S., and Ordal, G.W. (1991) Sequence and characterization of Bacillus subtilis CheB, a homolog of Escherichia coli CheY, and its role in a different mechanism of chemotaxis. J Biol Chem 266: 12301-12305.
4. Bischoff, D.S., Bourret, R.B., Kirsch, M.L., and Ordal, G.W. (1993) Purification and characterization of Bacillus subtilis CheY. Biochemistry 32: 9256-9261.
5. Borkovich, K.A., and Simon, M.I. (1990) The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63: 1339-1348.
6. Bornhorst, J.A., and Falke, J.J. (2001) Evidence that both ligand binding and covalent adaptation drive a two-state equilibrium in the aspartate receptor signaling complex. J Gen Physiol 118: 693-710.
7. Briegel, A., Ortega, D.R., Tocheva, E.I., Wuichet, K., Li, Z., Chen, S., etal. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106: 17181-17186.
8. Briegel, A., Wong, M.L., Hodges, H.L., Oikonomou, C.M., Piasta, K.N., Harris, M.J., etal. (2014) New insights into bacterial chemoreceptor array structure and assembly from electron cryotomography. Biochemistry 53: 1575-1585.
9. Burgess-Cassler, A., Ullah, A.H., and Ordal, G.W. (1982) Purification and characterization of Bacillus subtilis methyl-accepting chemotaxis protein methyltransferase II. J Biol Chem 257: 8412-8417.
10. Cannistraro, V.J., Glekas, G.D., Rao, C.V., and Ordal, G.W. (2011) Cellular stoichiometry of the chemotaxis proteins in Bacillus subtilis. J Bacteriol 193: 3220-3227.
11. Chao, X., Muff, T.J., Park, S.Y., Zhang, S., Pollard, A.M., Ordal, G.W., etal. (2006) A receptor-modifying deamidase in complex with a signaling phosphatase reveals reciprocal regulation. Cell 124: 561-571.
12. Conrad, B., Savchenko, R.S., Breves, R., and Hofemeister, J. (1996) A T7 promoter-specific, inducible protein expression system for Bacillus subtilis. Mol Gen Genet 250: 230-236.
13. Dunten, P., and Koshland, D.E., Jr (1991) Tuning the responsiveness of a sensory receptor via covalent modification. J Biol Chem 266: 1491-1496.
14. Earl, A.M., Losick, R., and Kolter, R. (2008) Ecology and genomics of Bacillus subtilis. Trends Microbiol 16: 269-275.
15. Fredrick, K.L., and Helmann, J.D. (1994) Dual chemotaxis signaling pathways in Bacillus subtilis: a sigma D-dependent gene encodes a novel protein with both CheW and CheY homologous domains. J Bacteriol 176: 2727-2735.
16. Garrity, L.F., and Ordal, G.W. (1997) Activation of the CheA kinase by asparagine in Bacillus subtilis chemotaxis. Microbiology 143: 2945-2951.
17. Gegner, J.A., Graham, D.R., Roth, A.F., and Dahlquist, F.W. (1992) Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70: 975-982.
18. Glekas, G.D., Foster, R.M., Cates, J.R., Estrella, J.A., Wawrzyniak, M.J., Rao, C.V., and Ordal, G.W. (2010) A PAS domain binds asparagine in the chemotaxis receptor McpB in Bacillus subtilis. J Biol Chem 285: 1870-1878.
19. Glekas, G.D., Cates, J.R., Cohen, T.M., Rao, C.V., and Ordal, G.W. (2011) Site-specific methylation in Bacillus subtilis chemotaxis: effect of covalent modifications to the chemotaxis receptor McpB. Microbiology 157: 56-65.
20. Glekas, G.D., Plutz, M.J., Walukiewicz, H.E., Allen, G.M., Rao, C.V., and Ordal, G.W. (2012) Elucidation of the multiple roles of CheD in Bacillus subtilis chemotaxis. Mol Microbiol 86: 743-756.
21. Goldman, D.J., Nettleton, D.O., and Ordal, G.W. (1984) Purification and characterization of chemotactic methylesterase from Bacillus subtilis. Biochemistry 23: 675-680.
22. Hanlon, D.W., and Ordal, G.W. (1994) Cloning and characterization of genes encoding methyl-accepting chemotaxis proteins in Bacillus subtilis. J Biol Chem 269: 14038-14046.
23. Hazelbauer, G.L., Falke, J.J., and Parkinson, J.S. (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9-19.
24. Hou, S., Larsen, R.W., Boudko, D., Riley, C.W., Karatan, E., Zimmer, M., etal. (2000) Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403: 540-544.
25. Karatan, E., Saulmon, M.M., Bunn, M.W., and Ordal, G.W. (2001a) Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J Biol Chem 276: 43618-43626.
26. Karatan, E., Saulmon, M.M., Bunn, M.W., and Ordal, G.W. (2001b) Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J Biol Chem 276: 43618-43626.
27. Kirby, J.R., Kristich, C.J., Feinberg, S.L., and Ordal, G.W. (1997) Methanol production during chemotaxis to amino acids in Bacillus subtilis. Mol Microbiol 24: 869-878.
28. Kirby, J.R., Saulmon, M.M., Kristich, C.J., and Ordal, G.W. (1999) CheY-dependent methylation of the asparagine receptor, McpB, during chemotaxis in Bacillus subtilis. J Biol Chem 274: 11092-11100.
29. Kristich, C.J., and Ordal, G.W. (2002) Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J Biol Chem 277: 25356-25362.
30. Lertsethtakarn, P., Ottemann, K.M., and Hendrixson, D.R. (2011) Motility and chemotaxis in Campylobacter and Helicobacter. Annu Rev Microbiol 65: 389-410.
31. Li, M., and Hazelbauer, G.L. (2004) Cellular stoichiometry of the components of the chemotaxis signaling complex. J Bacteriol 186: 3687-3694.
32. Macnab, R.M., and Koshland, D.E., Jr (1972) The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci USA 69: 2509-2512.
33. Muff, T.J., and Ordal, G.W. (2007) The CheC phosphatase regulates chemotactic adaptation through CheD. J Biol Chem 282: 34120-34128.
34. Pieper, R., Huang, S.T., Clark, D.J., Robinson, J.M., Alami, H., Parmar, P.P., etal. (2009) Integral and peripheral association of proteins and protein complexes with Yersinia pestis inner and outer membranes. Proteome Sci 7: 5.
35. Porter, S.L., Wadhams, G.H., and Armitage, J.P. (2011) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9: 153-165.
36. Quon, K.C., Marczynski, G.T., and Shapiro, L. (1996) Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84: 83-93.
37. Rao, C.V., and Ordal, G.W. (2009) The molecular basis of excitation and adaptation during chemotactic sensory transduction in bacteria. Contrib Microbiol 16: 33-64.
38. Rao, C.V., Kirby, J.R., and Arkin, A.P. (2004) Design and diversity in bacterial chemotaxis: a comparative study in Escherichia coli and Bacillus subtilis. PLoS Biol 2: E49.
39. Rao, C.V., Glekas, G.D., and Ordal, G.W. (2008) The three adaptation systems of Bacillus subtilis chemotaxis. Trends Microbiol 16: 480-487.
40. Rosario, M.M., Fredrick, K.L., Ordal, G.W., and Helmann, J.D. (1994) Chemotaxis in Bacillus subtilis requires either of two functionally redundant CheW homologs. J Bacteriol 176: 2736-2739.
41. Szurmant, H., and Ordal, G.W. (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68: 301-319.
42. Szurmant, H., Muff, T.J., and Ordal, G.W. (2004) Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J Biol Chem 279: 21787-21792.
43. Tan, S. (2001) A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr Purif 21: 224-234.
44. Ullah, A.H., and Ordal, G.W. (1981) In vivo and in vitro chemotactic methylation in Bacillus subtilis. J Bacteriol 145: 958-965.
45. Webb, M.R. (1992) A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc Natl Acad Sci USA 89: 4884-4887.
46. Wu, K., Walukiewicz, H.E., Glekas, G.D., Ordal, G.W., and Rao, C.V. (2011) Attractant binding induces distinct structural changes to the polar and lateral signaling clusters in Bacillus subtilis chemotaxis. J Biol Chem 286: 2587-2595.
47. Wuichet, K., and Zhulin, I.B. (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3: ra50.
48. Yuan, W., Glekas, G.D., Allen, G.M., Walukiewicz, H.E., Rao, C.V., and Ordal, G.W. (2012) The importance of the interaction of CheD with CheC and the chemoreceptors compared to its enzymatic activity during chemotaxis in Bacillus subtilis. PLoS ONE 7: e50689.
49. Zimmer, M.A., Tiu, J., Collins, M.A., and Ordal, G.W. (2000) Selective methylation changes on the Bacillus subtilis chemotaxis receptor McpB promote adaptation. J Biol Chem 275: 24264-24272.
50. Zimmer, M.A., Szurmant, H., Saulmon, M.M., Collins, M.A., Bant, J.S., and Ordal, G.W. (2002) The role of heterologous receptors in McpB-mediated signalling in Bacillus subtilis chemotaxis. Mol Microbiol 45: 555-568.