Specific gamma-aminobutyrate chemotaxis in pseudomonads with different lifestyle

Molecular Microbiology

Volumn 97, Issue 3, 2015, Pages 488-501

  Reyes Darias, Jose Antonio ^a   García, Vanina ^a   Rico Jiménez, Miriam ^a   Corral Lugo, Andrés ^a   Lesouhaitier, Olivier ^b   Juárez Hernández, Dalia ^c   Yang, Yiling ^d,e   Bi, Shuangyu ^d,e   Feuilloley, Marc ^b   Muñoz Rojas, Jesús ^c   Sourjik, Victor ^d,e   Krell, Tino ^a  

^a CSIC   (Spain)

^b UNIVERSITÉ DE ROUEN   (France)

^c BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; MCPG CHEMORECEPTOR; PCTC CHEMORECEPTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PCTC PROTEIN, PSEUDOMONAS AERUGINOSA; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL PLANT DISEASE; BACTERIAL VIRULENCE; CAENORHABDITIS ELEGANS; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; GENE DELETION; LIGAND BINDING; NONHUMAN; PLANT ROOT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PSEUDOMONAS PUTIDA; ROOT EXUDATE; SIGNAL TRANSDUCTION; SOIL MICROFLORA; TOMATO; ANIMAL; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; LYCOPERSICON ESCULENTUM; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

ANIMALS; BACTERIAL PROTEINS; CAENORHABDITIS ELEGANS; CHEMOTAXIS; GAMMA-AMINOBUTYRIC ACID; GENE DELETION; LYCOPERSICON ESCULENTUM; PLANT ROOTS; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PUTIDA; RECOMBINANT PROTEINS; VIRULENCE;

EID: 84937975622     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13045     Document Type: Article

References (76)

1. Abril, M.A., Michan, C., Timmis, K.N., and Ramos, J.L. (1989) Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway. J Bacteriol 171: 6782-6790.
2. Adler, J. (1966) Chemotaxis in bacteria. Science 153: 708-716.
3. Allan, W.L., Simpson, J.P., Clark, S.M., and Shelp, B.J. (2008) Gamma-hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms. J Exp Bot 59: 2555-2564.
4. Ames, P., Studdert, C.A., Reiser, R.H., and Parkinson, J.S. (2002) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060-7065.
5. Antunez-Lamas, M., Cabrera, E., Lopez-Solanilla, E., Solano, R., Gonzalez-Melendi, P., Chico, J.M., etal. (2009) Bacterial chemoattraction towards jasmonate plays a role in the entry of Dickeya dadantii through wounded tissues. Mol Microbiol 74: 662-671.
6. Badri, D.V., Chaparro, J.M., Zhang, R., Shen, Q., and Vivanco, J.M. (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288: 4502-4512.
7. Bagdasarian, M., Lurz, R., Ruckert, B., Franklin, F.C., Bagdasarian, M.M., Frey, J., and Timmis, K.N. (1981) Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. Gene 16: 237-247.
8. Bansal, T., Englert, D., Lee, J., Hegde, M., Wood, T.K., and Jayaraman, A. (2007) Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75: 4597-4607.
9. Barlow, R., and Blake, J.F. (1989) Hill coefficients and the logistic equation. Trends Pharmacol Sci 10: 440-441.
10. Blier, A.S., Veron, W., Bazire, A., Gerault, E., Taupin, L., Vieillard, J., etal. (2011) C-type natriuretic peptide modulates quorum sensing molecule and toxin production in Pseudomonas aeruginosa. Microbiology 157: 1929-1944.
11. Borkovich, K.A., Alex, L.A., and Simon, M.I. (1992) Attenuation of sensory receptor signaling by covalent modification. Proc Natl Acad Sci USA 89: 6756-6760.
12. Bouche, N., and Fromm, H. (2004) GABA in plants: just a metabolite? Trends Plant Sci 9: 110-115.
13. Bown, A.W., Macgregor, K.B., and Shelp, B.J. (2006) Gamma-aminobutyrate: defense against invertebrate pests? Trends Plant Sci 11: 424-427.
14. Buron-Barral, M.C., Gosink, K.K., and Parkinson, J.S. (2006) Loss- and gain-of-function mutations in the F1-HAMP region of the Escherichia coli aerotaxis transducer Aer. J Bacteriol 188: 3477-3486.
15. Cao, H., Baldini, R.L., and Rahme, L.G. (2001) Common mechanisms for pathogens of plants and animals. Annu Rev Phytopathol 39: 259-284.
16. Carvalhais, L.C., Dennis, P.G., Fedoseyenko, D., Hajirezaei, M.R., Borriss, R., and von Wirén, N. (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174: e68555.
17. Corral-Lugo, A., Morales-García, Y., Pazos-Rojas, L.A., Ramírez-Valverde, A., Martínez-Contreras, R.D., and Muñoz-Rojas, J. (2012) Quantification of cultivable bacteria by the Massive Stamping Drop Plate method. Rev Colomb Biotecnol 14: 173-182.
18. Dagorn, A., Hillion, M., Chapalain, A., Lesouhaitier, O., Duclairoir Poc, C., Vieillard, J., etal. (2013) Gamma-aminobutyric acid acts as a specific virulence regulator in Pseudomonas aeruginosa. Microbiology 159: 339-351.
19. Duque, E., Molina-Henares, A.J., de la Torre, J., Molina-Henares, M.A., del Castillo, T., Lam, J., and Ramos, J.L. (2007) Towards a genome-wide mutant library of pseudomonas putida strain KT2440. In Pseudomonas: A Model System in Biology, Vol. V. Ramos, J.L., and Filloux, A. (eds). Dorchester, The Netherlands: Springer, pp. 227-251.
20. El-Ansary, A.K., Ben Bacha, A., and Kotb, M. (2012) Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J Neuroinflammation 9: 74.
21. 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.
22. Espinosa-Urgel, M., Kolter, R., and Ramos, J.L. (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiology 148: 341-343.
23. 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.
24. Garvis, S., Munder, A., Ball, G., de Bentzmann, S., Wiehlmann, L., Ewbank, J.J., etal. (2009) Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. PLoS Pathog 5: e1000540.
25. 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.
26. Glekas, G.D., Mulhern, B.J., Kroc, A., Duelfer, K.A., Lei, V., Rao, C.V., and Ordal, G.W. (2012) The Bacillus subtilis chemoreceptor McpC senses multiple ligands using two discrete mechanisms. J Biol Chem 287: 39412-39418.
27. Grimm, A.C., and Harwood, C.S. (1997) Chemotaxis of Pseudomonas spp. to the polyaromatic hydrocarbon naphthalene. Appl Environ Microbiol 63: 4111-4115.
28. Harwood, C.S., Rivelli, M., and Ornston, L.N. (1984) Aromatic acids are chemoattractants for Pseudomonas putida. J Bacteriol 160: 622-628.
29. 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.
30. Hegde, M., Englert, D.L., Schrock, S., Cohn, W.B., Vogt, C., Wood, T.K., etal. (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.
31. Kato, J., Kim, H.E., Takiguchi, N., Kuroda, A., and Ohtake, H. (2008) Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. J Biosci Bioeng 106: 1-7.
32. Krell, T. (2008) Microcalorimetry: a response to challenges in modern biotechnology. Microb Biotechnol 1: 126-136.
33. Krell, T., Lacal, J., Busch, A., Silva-Jimenez, H., Guazzaroni, M.E., and Ramos, J.L. (2010) Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64: 539-559.
34. Kuroda, A., Kumano, T., Taguchi, K., Nikata, T., Kato, J., and Ohtake, H. (1995) Molecular cloning and characterization of a chemotactic transducer gene in Pseudomonas aeruginosa. J Bacteriol 177: 7019-7025.
35. Lacal, J., Alfonso, C., Liu, X., Parales, R.E., Morel, B., Conejero-Lara, F., etal. (2010a) Identification of a chemoreceptor for tricarboxylic acid cycle intermediates: differential chemotactic response towards receptor ligands. J Biol Chem 285: 23126-23136.
36. Lacal, J., Garcia-Fontana, C., Munoz-Martinez, F., Ramos, J.L., and Krell, T. (2010b) Sensing of environmental signals: classification of chemoreceptors according to the size of their ligand binding regions. Environ Microbiol 12: 2873-2884.
37. Matilla, M.A., Espinosa-Urgel, M., Rodriguez-Herva, J.J., Ramos, J.L., and Ramos-Gonzalez, M.I. (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol 8: R179.
38. Mesibov, R., and Adler, J. (1972) Chemotaxis toward amino acids in Escherichia coli. J Bacteriol 112: 315-326.
39. Milligan, D.L., and Koshland, D.E., Jr (1993) Purification and characterization of the periplasmic domain of the aspartate chemoreceptor. J Biol Chem 268: 19991-19997.
40. Morales-Garcia, Y.E., Juarez-Hernandez, D., Aragon-Hernandez, C., Mascarua-Esparza, M.A., Bustillos-Cristales, M.R., Fuentes-Ramirez, L.E., etal. (2011) Growth response of maize plantlets inoculated with Enterobacter spp., as a model for alternative agriculture. Rev Argent Microbiol 43: 287-293.
41. Mowbray, S.L., and Koshland, D.E., Jr (1987) Additive and independent responses in a single receptor: aspartate and maltose stimuli on the tar protein. Cell 50: 171-180.
42. Nahm, M., Radoglou, K., Halyvopoulos, G., Gessler, A., Rennenberg, H., and Fotelli, M.N. (2006) Physiological performance of beech (Fagus sylvatica L.) at its southeastern distribution limit in Europe: seasonal changes in nitrogen, carbon and water balance. Plant Biol (Stuttg) 8: 52-63.
43. Naresh, R., and Hampson, D.J. (2011) Exposure to norepinephrine enhances Brachyspira pilosicoli growth, attraction to mucin and attachment to Caco-2 cells. Microbiology 157: 543-547.
44. Neal, A.L., Ahmad, S., Gordon-Weeks, R., and Ton, J. (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS ONE 7: e35498.
45. Neumann, S., Hansen, C.H., Wingreen, N.S., and Sourjik, V. (2010) Differences in signalling by directly and indirectly binding ligands in bacterial chemotaxis. EMBO J 29: 3484-3495.
46. Neumann, S., Grosse, K., and Sourjik, V. (2012) Chemotactic signaling via carbohydrate phosphotransferase systems in Escherichia coli. Proc Natl Acad Sci USA 109: 12159-12164.
47. Oleksiuk, O., Jakovljevic, V., Vladimirov, N., Carvalho, R., Paster, E., Ryu, W.S., etal. (2011) Thermal robustness of signaling in bacterial chemotaxis. Cell 145: 312-321.
48. Pasupuleti, S., Sule, N., Cohn, W.B., MacKenzie, D.S., Jayaraman, A., and Manson, M.D. (2014) Chemotaxis of Escherichia coli to norepinephrine (NE) requires conversion of NE to 3, 4-dihydroxymandelic acid. J Bacteriol 196: 3992-4000.
49. Penrose, D.M., and Glick, B.R. (2001) Levels of ACC and related compounds in exudate and extracts of canola seeds treated with ACC deaminase-containing plant growth-promoting bacteria. Can J Microbiol 47: 368-372.
50. Rader, B.A., Wreden, C., Hicks, K.G., Sweeney, E.G., Ottemann, K.M., and Guillemin, K. (2011) Helicobacter pylori perceives the quorum-sensing molecule AI-2 as a chemorepellent via the chemoreceptor TlpB. Microbiology 157: 2445-2455.
51. Rahme, L.G., Stevens, E.J., Wolfort, S.F., Shao, J., Tompkins, R.G., and Ausubel, F.M. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
52. Regenhardt, D., Heuer, H., Heim, S., Fernandez, D.U., Strompl, C., Moore, E.R., and Timmis, K.N. (2002) Pedigree and taxonomic credentials of Pseudomonas putida strain KT2440. Environ Microbiol 4: 912-915.
53. Reyes Darias, J.A., Yang, Y., Sourjik, V., and Krell, T. (2015) Correlation between signal input and output in PctA and PctB amino acid chemoreceptor of Pseudomonas aeruginosa. Mol Microbiol. 96: 513-525.
54. Rico, A., and Preston, G.M. (2008) Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant Microbe Interact 21: 269-282.
55. Rico-Jimenez, M., Munoz-Martinez, F., Garcia-Fontana, C., Fernandez, M., Morel, B., Ortega, A., etal. (2013) Paralogous chemoreceptors mediate chemotaxis towards protein amino acids and the non-protein amino acid gamma-aminobutyrate (GABA). Mol Microbiol 88: 1230-1243.
56. Scott, J.C., Greenhut, I.V., and Leveau, J.H. (2013) Functional characterization of the bacterial iac genes for degradation of the plant hormone indole-3-acetic acid. J Chem Ecol 39: 942-951.
57. Shelp, B.J., Bown, A.W., and McLean, M.D. (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4: 446-452.
58. Shelp, B.J., Bown, A.W., and Faure, D. (2006) Extracellular gamma-aminobutyrate mediates communication between plants and other organisms. Plant Physiol 142: 1350-1352.
59. Shitashiro, M., Tanaka, H., Hong, C.S., Kuroda, A., Takiguchi, N., Ohtake, H., and Kato, J. (2005) Identification of chemosensory proteins for trichloroethylene in Pseudomonas aeruginosa. J Biosci Bioeng 99: 396-402.
60. Sourjik, V., and Berg, H.C. (2002a) Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc Natl Acad Sci USA 99: 12669-12674.
61. Sourjik, V., and Berg, H.C. (2002b) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99: 123-127.
62. Sourjik, V., and Berg, H.C. (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428: 437-441.
63. Sourjik, V., Vaknin, A., Shimizu, T.S., and Berg, H.C. (2007) In vivo measurement by FRET of pathway activity in bacterial chemotaxis. Methods Enzymol 423: 365-391.
64. Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P., and Kaper, J.B. (2003) Bacteria-host communication: the language of hormones. Proc Natl Acad Sci USA 100: 8951-8956.
65. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., etal. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
66. Straub, R.H., Wiest, R., Strauch, U.G., Harle, P., and Scholmerich, J. (2006) The role of the sympathetic nervous system in intestinal inflammation. Gut 55: 1640-1649.
67. 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.
68. Taguchi, K., Fukutomi, H., Kuroda, A., Kato, J., and Ohtake, H. (1997) Genetic identification of chemotactic transducers for amino acids in Pseudomonas aeruginosa. Microbiology 143 (Part 10): 3223-3229.
69. Tan, M.W., Mahajan-Miklos, S., and Ausubel, F.M. (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci USA 96: 715-720.
70. Tawaraya, K., Horie, R., Saito, S., Wagatsuma, T., Saito, K., and Oikawa, A. (2014) Metabolite profiling of root exudates of common bean under phosphorus deficiency. Metabolites 4: 599-611.
71. Taylor, B.L., Miller, J.B., Warrick, H.M., and Koshland, D.E., Jr (1979) Electron acceptor taxis and blue light effect on bacterial chemotaxis. J Bacteriol 140: 567-573.
72. Tully, R.E., and Hanson, A.D. (1979) Amino acids translocated from turgid and water-stressed barley leaves: I. Phloem exudation studies. Plant Physiol 64: 460-466.
73. Utari, P.D., and Quax, W.J. (2013) Caenorhabditis elegans reveals novel Pseudomonas aeruginosa virulence mechanism. Trends Microbiol 21: 315-316.
74. Walker, T.S., Bais, H.P., Deziel, E., Schweizer, H.P., Rahme, L.G., Fall, R., and Vivanco, J.M. (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol 134: 320-331.
75. Woodcock, D.M., Crowther, P.J., Doherty, J., Jefferson, S., DeCruz, E., Noyer-Weidner, M., etal. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17: 3469-3478.
76. Wuichet, K., and Zhulin, I.B. (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3: ra50.