Characterization of the Thermotoga maritima chemotaxis methylation system that lacks pentapeptide-dependent methyltransferase CheR:MCP tethering

Molecular Microbiology

Volumn 63, Issue 2, 2007, Pages 363-378

  Perez, Eduardo ^a,b   Stock, Ann M ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLTRANSFERASE; PENTAPEPTIDE;

ADAPTATION; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CHEMOTAXIS; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SALMONELLA ENTERICA; SEQUENCE ANALYSIS; THERMOTOGA MARITIMA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CHEMOTAXIS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; KINETICS; MEMBRANE PROTEINS; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SALMONELLA ENTERICA; SEQUENCE HOMOLOGY, AMINO ACID; THERMOTOGA MARITIMA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROTEOBACTERIA; SALMONELLA ENTERICA; THERMOTOGA MARITIMA;

EID: 33846119340     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05518.x     Document Type: Article

References (92)

1. Alley, M.R.K., Maddock, J.R., and Shapiro, L. (1992) Polar localization of a bacterial chemoreceptor. Genes Dev 6: 825-836.
2. Anand, G.S., and Stock, A.M. (2002) Kinetic basis for the stimulatory effect of phosphorylation on the methylesterase activity of CheB. Biochemistry 41: 6752-6760.
3. Antommattei, F.M., and Weis, R.M. (2006) Reversible methylation of glutamate residues in the receptor proteins of bacterial sensory systems. In The Enzymes: Protein Methyltransferases, vol. 24. Clarke S.G. and Tamanoi F. (eds). San Diego: Academic Press pp. 325-381.
4. Armitage, J.P., and Schmitt, R. (1997) Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti-variations on a theme? Microbiology 143: 3671-3682.
5. Astling, D.P., Lee, J.Y., and Zusman, D.R. (2006) Differential effects of chemoreceptor methylation-domain mutations on swarming and development in the social bacterium Myxococcus xanthus. Mol Microbiol 59: 45-55.
6. Banno, S., Shiomi, D., Homma, M., and Kawagishi, I. (2004) Targeting of the chemotaxis methylesterase/deamidase CheB to the polar receptor-kinase cluster in an Escherichia coli cell. Mol Microbiol 53: 1051-1063.
7. Bardy, S.L., and Maddock, J.R. (2005) Polar localization of a soluble methyl-accepting protein of Pseudomonas aeruginosa. J Bacteriol 187: 7840-7844.
8. Barnakov, A.N., Barnakova, L.A., and Hazelbauer, G.L. (1998) Comparison in vitro of a high- and a low-abundance chemoreceptor of Escherichia coli: similar kinase activation but different methyl-accepting activities. J Bacteriol 180: 6713-6718.
9. Barnakov, A.N., Barnakova, L.A., and Hazelbauer, G.L. (1999) Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc Natl Acad Sci USA 96: 10667-10672.
10. Bhandari, P., and Gowrishankar, J. (1997) An Escherichia coli host strain useful for efficient overproduction of cloned gene products with NaCl as the inducer. J Bacteriol 179: 4403-4406.
11. Bilwes, A.M., Alex, L.A., Crane, B.R., and Simon, M.I. (1999) Structure of CheA, a signal-transducing histidine kinase. Cell 96: 131-141.
12. Bilwes, A.M., Quezada, C.M., Croal, L.R., Crane, B.R., and Simon, M.I. (2001) Nucleotide binding by the histidine kinase CheA. Nat Struct Biol 8: 353-360.
13. Blatch, G.L., and Lassle, M. (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21: 932-939.
14. Blom, N., Sicheritz-Ponten, T., Gupta, R., Gammeltoft, S., and Brunak, S. (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4: 1633-1649.
15. 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.
16. Bourret, R.B., and Stock, A.M. (2002) Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277: 9625-9628.
17. Bren, A., and Eisenbach, M. (2000) How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J Bacteriol 182: 6865-6873.
18. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921.
19. Burgess-Cassler, A., and Ordal, G.W. (1982) Functional homology of Bacillus subtilis methyltransferase II and Escherichia coli CheR protein. J Biol Chem 257: 12835-12838.
20. Bustamante, V.H., Martinez-Flores, I., Vlamakis, H.C., and Zusman, D.R. (2004) Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol Microbiol 53: 1501-1513.
21. Cantwell, B.J., Draheim, R.R., Weart, R.B., Nguyen, C., Stewart, R.C., and Manson, M.D. (2003) CheZ phosphatase localizes to chemoreceptor patches via CheA-short. J Bacteriol 185: 2354-2361.
22. Chao, X., Muff, T., Park, S., Zhang, S., Pollard, A.M., Ordal, G., et al. (2006) A receptor-modifying deamidase in complex with a signaling phosphatase reveals reciprocal regulation. Cell 124: 561-571.
23. Cuff, J.A., Clamp, M.E., Siddiqui, A.S., Finlay, M., and Barton, G.J. (1998) JPred: a consensus secondary structure prediction server. Bioinformatics 14: 892-893.
24. Das, A.K., Cohen, P.W., and Barford, D. (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J 17: 1192-1199.
25. Delano, W.L. (2002) The Pymol Molecular Graphics System. San Carlos, CA: DeLano Scientific.
26. Diemand, A.V., and Scheib, H. (2004) iMolTalk: an interactive, internet-based protein structure analysis server. Nucleic Acids Res 32: W512-W516.
27. Djordjevic, S., and Stock, A.M. (1997) Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine. Structure 5: 545-558.
28. Djordjevic, S., and Stock, A.M. (1998) Chemotaxis receptor recognition by methyltransferase CheR. Nat Struct Biol 5: 446-450.
29. Falke, J.J., and Hazelbauer, G.L. (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26: 257-265.
30. Falke, J.J., and Kim, S.H. (2000) Structure of a conserved receptor domain that regulates kinase activity: the cytoplasmic domain of bacterial taxis receptors. Curr Opin Struct Biol 10: 462-469.
31. Falke, J.J., Bass, R.B., Butler, S.L., Chervitz, S.A., and Danielson, M.A. (1997) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu Rev Cell Dev Biol 13: 457-512.
32. Feng, X., Baumgartner, J.W., and Hazelbauer, G.L. (1997) High- and low-abundance chemoreceptors in Escherichia coli: differential activities associated with closely related cytoplasmic domains. J Bacteriol 179: 6714-6720.
33. Feng, X., Lilly, A.A., and Hazelbauer, G.L. (1999) Enhanced function conferred on low-abundance chemoreceptor Trg by a methyltransferase-docking site. J Bacteriol 181: 3164-3171.
34. Galperin, M.Y. (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5: 35.
35. Glaser, F., Pupko, T., Paz, I., Bell, R.E., Bechor-Shental, D., Martz, E., and Ben-Tal, N. (2003) ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19: 163-164.
36. Griswold, I.J., Zhou, H., Swanson, R.V., McIntosh, L.P., Simon, M.I., and Dahlquist, F.W. (2002) The solution structure and interactions of CheW from Thermotoga maritima. Nat Struct Biol 9: 121-125.
37. 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.
38. Kehry, M.R., and Dahlquist, F.W. (1982) The methyl-accepting chemotaxis proteins of Escherichia coli. Identification of the multiple methylation sites on methyl-accepting chemotaxis protein I. J Biol Chem 257: 10378-10386.
39. Khidekel, N., and Hsieh-Wilson, L.C. (2004) A 'molecular switchboard' - covalent modifications to proteins and their impact on transcription. Org Biomol Chem 2: 1-7.
40. Kim, K.K., Yokota, H., and Kim, S.-H. (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400: 787-792.
41. 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: 11092-12100.
42. Kirby, J.R., Niewold, T.B., Maloy, S., and Ordal, G.W. (2000) CheB is required for behavioural responses to negative stimuli during chemotaxis in Bacillus subtilis. Mol Microbiol 35: 44-57.
43. 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.
44. Lamb, J.R., Tugendreich, S., and Hieter, P. (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem Sci 20: 257-259.
45. Le Moual, H., and Koshland, D.E., Jr (1996) Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis. J Mol Biol 261: 568-585.
46. Le Moual, H., Quang, T., and Koshland, D.E., Jr (1997) Methylation of the Escherichia coli chemotaxis receptors: intra- and interdimer mechanisms. Biochemistry 36: 13441-13448.
47. Li, M., and Hazelbauer, G.L. (2005) Adaptational assistance in clusters of bacterial chemoreceptors. Mol Microbiol 56: 1617-1626.
48. Li, M., and Hazelbauer, G.L. (2006) The carboxyl-terminal linker is important for chemoreceptor function. Mol Microbiol 60: 469-479.
49. Li, J., Li, G., and Weis, R.M. (1997) The serine chemoreceptor from Escherichia coli is methylated through an interdimer process. Biochemistry 36: 11851-11857.
50. Liu, J.D., and Parkinson, J.S. (1989) Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis. Proc Natl Acad Sci USA 86: 8703-8707.
51. Lybarger, S.R., and Maddock, J.R. (2001) Polarity in action: asymmetric protein localization in bacteria. J Bacteriol 183: 3261-3267.
52. Maddock, J.R., and Shapiro, L. (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717-1723.
53. Martin, A.C., Wadhams, G.H., Shah, D.S., Porter, S.L., Mantotta, J.C., Craig, T.J., et al. (2001) CheR- and CheB-dependent chemosensory adaptation system of Rhodobacter sphaeroides. J Bacteriol 183: 7135-7144.
54. Nelson, K.E., Clayton, R.A., Gill, S.R., Gwinn, M.L., Dodson, R.J., Haft, D.H., et al. (1999) Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399: 323-329.
55. Okumura, H., Nishiyama, S., Sasaki, A., Homma, M., and Kawagishi, I. (1998) Chemotactic adaptation is altered by changes in the carboxy-terminal sequence conserved among the major methyl-accepting chemoreceptors. J Bacteriol 180: 1862-1868.
56. Park, S., Borbat, P.P., Gonzalez-Bonet, G., Bhatnagar, J., Pollard, A.M., Freed, J.H., et al. (2006) Reconstruction of the chemotaxis receptor-kinase assembly. Nat Struct Mol Biol 13: 382-384.
57. Park, S.Y., Beel, B.D., Simon, M.I., Bilwes, A.M., and Crane, B.R. (2004a) In different organisms, the mode of interaction between two signaling proteins is not necessarily conserved. Proc Natl Acad Sci USA 101: 11646-11651.
58. Park, S.Y., Chao, X., Gonzalez-Bonet, G., Beel, B.D., Bilwes, A.M., and Crane, B.R. (2004b) Structure and function of an unusual family of protein phosphatases: the bacterial chemotaxis proteins CheC and CheX. Mol Cell 16: 563-574.
59. Perazzona, B., and Spudich, J.L. (1999) Identification of methylation sites and effects of phototaxis stimuli on transducer methylation in Halobacterium salinarum. J Bacteriol 181: 5676-5683.
60. Perez, E. (2006) Characterization of methyltransferase CheR interactions and methylation of chemoreceptors in S. enterica and T. maritima. PhD Dissertation. Piscataway, NJ: University of Medicine and Dentistry of New Jersey and Rutgers, The State University of New Jersey.
61. Perez, E., West, A.H., Stock, A.M., and Djordjevic, S. (2004) Discrimination between different methylation states of chemotaxis receptor Tar by receptor methyltransferase CheR. Biochemistry 43: 9539-9561.
62. Perez, E., Zheng, H., and Stock, A.M. (2006) Identification of methylation sites in Thermotoga maritima chemotaxis receptors. J Bacteriol 188: 4093-4100.
63. Porter, S.L., Warren, A.V., Martin, A.C., and Armitage, J.P. (2002) The third chemotaxis locus of Rhodobacter sphaeroides is essential for chemotaxis. Mol Microbiol 46: 1081-1094.
64. Quezada, C.M., Gradinaru, C., Simon, M.I., Bilwes, A.M., and Crane, B.R. (2004) Helical shifts generate two distinct conformers in the atomic resolution structure of the CheA phosphotransferase domain from Thermotoga maritima. J Mol Biol 341: 1283-1294.
65. 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.
66. Rosario, M.M., Kirby, J.R., Bochar, D.A., and Ordal, G.W. (1995) Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD. Biochemistry 34: 3823-3831.
67. Rosario, M.M.L., and Ordal, G.W. (1996) CheC and CheD interact to regulate methylation of Bacillus subtilis methyl-accepting chemotaxis proteins. Mol Microbiol 21: 511-518.
68. Schneider, T.D., and Stephens, R.M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18: 6097-6100.
69. Shiomi, D., Okumura, H., Homma, M., and Kawagishi, I. (2000) The aspartate chemoreceptor Tar is effectively methylated by binding to the methyltransferase mainly through hydrophobic interaction. Mol Microbiol 36: 132-140.
70. Shiomi, D., Zhulin, I.B., Homma, M., and Kawagishi, I. (2002a) Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem 277: 42325-42333.
71. Shiomi, D., Homma, M., and Kawagishi, I. (2002b) Intragenic suppressors of a mutation in the aspartate chemoreceptor gene that abolishes binding of the receptor to methyltransferase. Microbiology 148: 3265-3275.
72. Simms, S.A., and Subbaramaiah, K. (1991) The kinetic mechanism of S-adenosyl-L-methionine: glutamylmethyl-transferase from Salmonella typhimurium. J Biol Chem 266: 12741-12746.
73. Simms, S.A., Keane, M.G., and Stock, J. (1985) Multiple forms of the CheB methylesterase in bacterial chemosensing. J Biol Chem 260: 10161-10168.
74. Simms, S.A., Stock, A.M., and Stock, J.B. (1987) Purification and characterization of the S-adenosylmethionine: glutamyl methyltransferase that modifies membrane chemoreceptor proteins in bacteria. J Biol Chem 262: 8537-8543.
75. Sourjik, V., and Berg, H.C. (2000) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37: 740-751.
76. Springer, W.R., and Koshland, D.E., Jr (1977) Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc Natl Acad Sci USA 74: 533-537.
77. Stock, J.B., and Koshland, D.E., Jr (1978) A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci USA 75: 3659-3663.
78. Swanson, R.V., Sanna, M.G., and Simon, M.I. (1996) Thermostable chemotaxis proteins from the hyperthermophilic bacterium Thermotoga maritima. J Bacteriol 178: 484-489.
79. Szurmant, H., and Ordal, G.W. (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68: 301-319.
80. Tabor, S., and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 84: 1074-1078.
81. Taylor, B.L., and Zhulin, I.B. (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63: 479-506.
82. Terwilliger, T.C., and Koshland, D.E., Jr (1984) Sites of methyl-esterification and deamination on the aspartate receptor involved in chemotaxis. J Biol Chem 259: 7719-7725.
83. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
84. Usher, K.C., de la Cruz, A.F., Dahlquist, F.W., Swanson, R.V., Simon, M.I., and Remington, S.J. (1998) Crystal structures of CheY from Thermotoga maritima do not support conventional explanations for the structural basis of enhanced thermostability. Protein Sci 7: 403-412.
85. Wadhams, G.H., and Armitage, J.P. (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
86. Wadhams, G.H., Martin, A.C., Porter, S.L., Maddock, J.R., Mantotta, J.C., King, H.M., and Armitage, J.P. (2002) TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol Microbiol 46: 1211-1221.
87. Wadhams, G.H., Martin, A.C., Warren, A.V., and Armitage, J.P. (2005) Requirements for chemotaxis protein localization in Rhodobacter sphaeroides. Mol Microbiol 58: 895-902.
88. Ward, M.J., and Zusman, D.R. (1997) Regulation of directed motility in Myxococcus xanthus. Mol Microbiol 24: 885-893.
89. Wolfe, A.J., Conley, M.P., Kramer, T.J., and Berg, H.C. (1987) Reconstitution of signaling in bacterial chemotaxis. J Bacteriol 169: 1878-1885.
90. Wu, J., Li, J., Li, G., Long, D.G., and Weis, R.M. (1996) The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35: 4984-4993.
91. Zhulin, I.B. (2001) The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv Microb Physiol 45: 157-198.
92. 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.