High specificity in CheR methyltransferase function: CheR2 of pseudomonas putida is essential for chemotaxis, whereas CheR1 is involved in biofilm formation

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 18987-18999

  García Fontana, Cristina ^a   Reyes Darias, José Antonio ^a,b   Muñoz Martínez, Francisco ^a   Alfonso, Carlos ^c   Morel, Bertrand ^d   Ramos, Juan Luis ^a   Krell, Tino ^a  

^a CSIC   (Spain)

^b Bio Iliberis R and D   (Spain)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^d UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL ULTRACENTRIFUGATION; COMPARATIVE ANALYSIS; DEGREE OF SPECIFICITY; ISOTHERMAL TITRATION CALORIMETRY; METHYLATION REACTION; S-ADENOSYLHOMOCYSTEINE; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION MECHANISM;

ALKYLATION; BIOFILMS; ESCHERICHIA COLI; METHYLATION; PHYSIOLOGY; SALMONELLA; SIGNAL TRANSDUCTION;

BIOCHEMISTRY;

CHER METHYLTRANSFERASE; CHER1 PROTEIN; CHER2 PROTEIN; MCPS PROTEIN; MCPT PROTEIN; METHYLTRANSFERASE; MONOMER; PENTAPEPTIDE; RECEPTOR; S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BINDING AFFINITY; BIOFILM; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; MCPS GENE; MCPT GENE; METHYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN UNFOLDING; PSEUDOMONAS PUTIDA; ULTRACENTRIFUGATION;

CALORIMETRY; CHEMORECEPTOR; CHEMOTAXIS; CHER METHYLTRANSFERASE; PROTEIN METHYLATION; PSEUDOMONAS; RECEPTOR MODIFICATION; RECEPTORS; S-ADENOSYLMETHIONINE (SAM); SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOFILMS; CALORIMETRY; CHEMOTAXIS; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; MUTATION; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PSEUDOMONAS PUTIDA; S-ADENOSYLMETHIONINE; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; ULTRACENTRIFUGATION;

ESCHERICHIA COLI; PSEUDOMONAS PUTIDA; SALMONELLA TYPHIMURIUM;

EID: 84879579504     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.472605     Document Type: Article

References (69)

1. 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
2. Ulrich, L. E., Koonin, E. V., and Zhulin, I. B. (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13, 52-56 (Pubitemid 40174862)
3. Wuichet, K., and Zhulin, I. B. (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci. Signal 3, ra50
4. Sourjik, V., and Wingreen, N. S. (2012) Responding to chemical gradients. Bacterial chemotaxis. Curr. Opin. Cell Biol. 24, 262-268
5. 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
6. Yuan, J., Branch, R. W., Hosu, B. G., and Berg, H. C. (2012) Adaptation at the output of the chemotaxis signalling pathway. Nature 484, 233-236
7. Min, T. L., Mears, P. J., Golding, I., and Chemla, Y. R. (2012) Chemotactic adaptation kinetics of individual Escherichia coli cells. Proc. Natl. Acad. Sci. U.S.A. 109, 9869-9874
8. Lazova, M. D., Ahmed, T., Bellomo, D., Stocker, R., and Shimizu, T. S. (2011) Response rescaling in bacterial chemotaxis. Proc. Natl. Acad. Sci. U.S.A. 108, 13870-13875
9. Vladimirov, N., and Sourjik, V. (2009) Chemotaxis. How bacteria use memory. Biol. Chem. 390, 1097-1104
10. Stock, J. B., Maderis, A. M., and Koshland, D. E., Jr. (1981) Bacterial chemotaxis in the absence of receptor carboxylmethylation. Cell 27, 37-44 (Pubitemid 12205969)
11. Wong, L. S., Johnson, M. S., Zhulin, I. B., and Taylor, B. L. (1995) Role of methylation in aerotaxis in Bacillus subtilis. J. Bacteriol. 177, 3985-3991
12. Stephens, B. B., Loar, S. N., and Alexandre, G. (2006) Role of CheB and CheR in the complex chemotactic and aerotactic pathway of Azospirillum brasilense. J. Bacteriol. 188, 4759-4768 (Pubitemid 43956074)
13. Kanungpean, D., Kakuda, T., and Takai, S. (2011) Participation of CheR and CheB in the chemosensory response of Campylobacter jejuni. Microbiology 157, 1279-1289
14. Ely, B., Gerardot, C. J., Fleming, D. L., Gomes, S. L., Frederikse, P., and Shapiro, L. (1986) General nonchemotactic mutants of Caulobacter crescentus. Genetics 114, 717-730
15. Borkovich, K. A., Alex, L. A., and Simon, M. I. (1992) Attenuation of sensory receptor signaling by covalent modification. Proc. Natl. Acad. Sci. U.S.A. 89, 6756-6760
16. 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 (Pubitemid 14081185)
17. Li, G., and Weis, R. M. (2000) Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100, 357-365 (Pubitemid 30353091)
18. Simms, S. A., and Subbaramaiah, K. (1991) The kinetic mechanism of S-adenosyl-L-methionine. Glutamylmethyltransferase from Salmonella typhimurium. J. Biol. Chem. 266, 12741-12746 (Pubitemid 21907157)
19. Yi, X., and Weis, R. M. (2002) The receptor docking segment and S-adenosyl-L-homocysteine bind independently to the methyltransferase of bacterial chemotaxis. Biochim. Biophys. Acta 1596, 28-35 (Pubitemid 34450837)
20. 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
21. Djordjevic, S., and Stock, A. M. (1998) Chemotaxis receptor recognition by protein methyltransferase CheR. Nat. Struct. Biol. 5, 446-450 (Pubitemid 28265027)
22. Muppirala, U. K., Desensi, S., Lybrand, T. P., Hazelbauer, G. L., and Li, Z. (2009) Molecular modeling of flexible arm-mediated interactions between bacterial chemoreceptors and their modification enzyme. Protein Sci. 18, 1702-1714
23. Krell, T., Lacal, J., Muñoz-Martínez, F., Reyes-Darias, J. A., Cadirci, B. H., García-Fontana, C., and Ramos, J. L. (2011) Diversity at its best. Bacterial taxis. Environ. Microbiol. 13, 1115-1124
24. Hamer, R., Chen, P. Y., Armitage, J. P., Reinert, G., and Deane, C. M. (2010) Deciphering chemotaxis pathways using cross species comparisons. BMC Syst. Biol. 4, 3
25. Lacal, J., García-Fontana, C., Muñoz-Martínez, F., Ramos, J. L., and Krell, T. (2010) Sensing of environmental signals. Classification of chemoreceptors according to the size of their ligand binding regions. Environ. Microbiol. 12, 2873-2884
26. Zhulin, I. B. (2001) The superfamily of chemotaxis transducers. From physiology to genomics and back. Adv. Microb. Physiol. 45, 157-198
27. 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 (Pubitemid 26335947)
28. Ferrández, A., Hawkins, A. C., Summerfield, D. T., and Harwood, C. S. (2002) Cluster II che genes from Pseudomonas aeruginosa are required for an optimal chemotactic response. J. Bacteriol. 184, 4374-4383
29. Masduki, A., Nakamura, J., Ohga, T., Umezaki, R., Kato, J., and Ohtake, H. (1995) Isolation and characterization of chemotaxis mutants and genes of Pseudomonas aeruginosa. J. Bacteriol. 177, 948-952
30. Kato, J., Nakamura, T., Kuroda, A., and Ohtake, H. (1999) Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem. 63, 155-161 (Pubitemid 129555252)
31. Hickman, J. W., Tifrea, D. F., and Harwood, C. S. (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. U.S.A. 102, 14422-14427 (Pubitemid 41429713)
32. Fulcher, N. B., Holliday, P. M., Klem, E., Cann, M. J., and Wolfgang, M. C. (2010) The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity. Mol. Microbiol. 76, 889-904
33. Darzins, A. (1994) Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility. Sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus. Mol. Microbiol. 11, 137-153
34. Kearns, D. B., Robinson, J., and Shimkets, L. J. (2001) Pseudomonas aeruginosa exhibits directed twitching motility up phosphatidylethanolamine gradients. J. Bacteriol. 183, 763-767 (Pubitemid 32048137)
35. Timmis, K. N. (2002) Pseudomonas putida. A cosmopolitan opportunist par excellence. Environ. Microbiol. 4, 779-781
36. Ramos, J. L., Krell, T., Daniels, C., Segura, A., and Duque, E. (2009) Responses of Pseudomonas to small toxic molecules by a mosaic of domains. Curr. Opin. Microbiol. 12, 215-220
37. Lacal, J., Reyes-Darias, J. A., García-Fontana, C., Ramos, J. L., and Krell, T. (2013) Tactic responses to pollutants and their potential to increase biodegradation efficiency. J. Appl. Microbiol. 114, 923-933
38. Lacal, J., Muñoz-Martínez, F., Reyes-Darías, J. A., Duque, E., Matilla, M., Segura, A., Calvo, J. J., Jímenez-Sánchez, C., Krell, T., and Ramos, J. L. (2011) Bacterial chemotaxis towards aromatic hydrocarbons in Pseudomonas. Environ. Microbiol. 13, 1733-1744
39. Lacal, J., Alfonso, C., Liu, X., Parales, R. E., Morel, B., Conejero-Lara, F., Rivas, G., Duque, E., Ramos, J. L., and Krell, T. (2010) Identification of a chemoreceptor for tricarboxylic acid cycle intermediates. Differential chemotactic response towards receptor ligands. J. Biol. Chem. 285, 23126-23136
40. Lacal, J., García-Fontana, C., Callejo-García, C., Ramos, J. L., and Krell, T. (2011) Physiologically relevant divalent cations modulate citrate recognition by the McpS chemoreceptor. J. Mol. Recognit. 24, 378-385
41. Pineda-Molina, E., Reyes-Darias, J. A., Lacal, J., Ramos, J. L., García-Ruiz, J. M., Gavira, J. A., and Krell, T. (2012) Evidence for chemoreceptors with bimodular ligand-binding regions harboring two signal-binding sites. Proc. Natl. Acad. Sci. U.S.A. 109, 18926-18931
42. Muñoz-Martínez, F., García-Fontana, C., Rico-Jiménez, M., Alfonso, C., and Krell, T. (2012) Genes encoding Cher-TPR fusion proteins are predominantly found in gene clusters encoding chemosensory pathways with alternative cellular functions. PLoS One 7, e45810
43. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179, 131-137 (Pubitemid 19149635)
44. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
45. Jones, K. S., Coleman, J., Merkel, G. W., Laue, T. M., and Skalka, A. M. (1992) Retroviral integrase functions as a multimer and can turn over catalytically. J. Biol. Chem. 267, 16037-16040
46. Stock, J. B., Clarke, S., and Koshland, D. E., Jr. (1984) The protein carboxylmethyltransferase involved in Escherichia coli and Salmonella typhimurium chemotaxis. Methods Enzymol. 106, 310-321
47. Campillo, J. E., and Ashcroft, S. J. (1982) Protein carboxymethylation in rat islets of Langerhans. FEBS Lett. 138, 71-75 (Pubitemid 12159349)
48. Duque, E., García, V., de la Torre, J., Godoy, P., Bernal, P., and Ramos, J. L. (2004) Plasmolysis induced by toluene in a cyoB mutant of Pseudomonas putida. Environ. Microbiol. 6, 1021-1031
49. Fellay, R., Frey, J., and Krisch, H. (1987) Interposon mutagenesis of soil and water bacteria. A family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52, 147-154 (Pubitemid 17090743)
50. O'Toole, G. A., Pratt, L. A., Watnick, P. I., Newman, D. K., Weaver, V. B., and Kolter, R. (1999) Genetic approaches to study of biofilms. Methods Enzymol. 310, 91-109 (Pubitemid 29504270)
51. 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 (Pubitemid 27191230)
52. Shiomi, D., Zhulin, I. B., Homma, M., and Kawagishi, I. (2002) Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J. Biol. Chem. 277, 42325-42333 (Pubitemid 35257553)
53. Krell, T. (2008) Microcalorimetry. A response to challenges in modern biotechnology. Microb. Biotechnol 1, 126-136
54. Turnbull, W. B., and Daranas, A. H. (2003) On the value of c. Can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866 (Pubitemid 37475576)
55. O'Connor, J. R., Kuwada, N. J., Huangyutitham, V., Wiggins, P. A., and Harwood, C. S. (2012) Surface sensing and lateral subcellular localization of WspA, the receptor in a chemosensory-like system leading to c-di-GMP production. Mol. Microbiol. 86, 720-729
56. Bantinaki, E., Kassen, R., Knight, C. G., Robinson, Z., Spiers, A. J., and Rainey, P. B. (2007) Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 176, 441-453 (Pubitemid 350021038)
57. Fillet, S., Krell, T., Morel, B., Lu, D., Zhang, X., and Ramos, J. L. (2011) Intramolecular signal transmission in a tetrameric repressor of the IclR family. Proc. Natl. Acad. Sci. U.S.A. 108, 15372-15377
58. Kedracka-Krok, S., and Wasylewski, Z. (2003) A differential scanning calorimetry study of tetracycline repressor. Eur. J. Biochem. 270, 4564-4573 (Pubitemid 37452533)
59. Błaszczyk, U., and Wasylewski, Z. (2003) Interaction of cAMP receptor protein from Escherichia coli with cAMP and DNA studied by differential scanning calorimetry. J. Protein Chem. 22, 285-293
60. Molina, L., Duque, E., Gómez, M. J., Krell, T., Lacal, J., García-Puente, A., García, V., Matilla, M. A., Ramos, J. L., and Segura, A. (2011) The pGRT1 plasmid of Pseudomonas putida DOT-T1E encodes functions relevant for survival under harsh conditions in the environment. Environ. Microbiol. 13, 2315-2327
61. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2008) Phylogeny.fr. Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469
62. Nelson, K. E., Weinel, C., Paulsen, I. T., Dodson, R. J., Hilbert, H., Martins dos Santos, V. A., Fouts, D. E., Gill, S. R., Pop, M., Holmes, M., Brinkac, L., Beanan, M., DeBoy, R. T., Daugherty, S., Kolonay, J., Madupu, R., Nelson, W., White, O., Peterson, J., Khouri, H., Hance, I., Chris Lee, P., Holtzapple, E., Scanlan, D., Tran, K., Moazzez, A., Utterback, T., Rizzo, M., Lee, K., Kosack, D., Moestl, D., Wedler, H., Lauber, J., Stjepandic, D., Hoheisel, J., Straetz, M., Heim, S., Kiewitz, C., Eisen, J. A., Timmis, K. N., Düsterhöft, A., Tümmler, B., and Fraser, C. M. (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4, 799-808 (Pubitemid 36064171)
63. Ramos, J. L., Duque, E., Huertas, M. J., and Haïdour, A. (1995) Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons. J. Bacteriol. 177, 3911-3916
64. Espinosa-Urgel, M., and Ramos, J. L. (2004) Cell density-dependent gene contributes to efficient seed colonization by Pseudomonas putida KT2440. Appl. Environ. Microbiol. 70, 5190-5198 (Pubitemid 39279589)
65. Studier, F. W., and Moffatt, B. A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113-130
66. Miroux, B., and Walker, J. E. (1996) Over-production of proteins in Escherichia coli. Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
67. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580
68. Rodríguez-Herva, J. J., García, V., Hurtado, A., Segura, A., and Ramos, J. L. (2007) The ttgGHI solvent efflux pump operon of Pseudomonas putida DOT-T1E is located on a large self-transmissible plasmid. Environ. Microbiol. 9, 1550-1561
69. Llamas, M. A., Rodríguez-Herva, J. J., Hancock, R. E., Bitter, W., Tommassen, J., and Ramos, J. L. (2003) Role of Pseudomonas putida tol-oprL gene products in uptake of solutes through the cytoplasmic membrane. J. Bacteriol. 185, 4707-4716