Taxis of Pseudomonas putida F1 toward phenylacetic acid is mediated by the energy taxis receptor AER2

Applied and Environmental Microbiology

Volumn 79, Issue 7, 2013, Pages 2416-2423

  Luu, Rita A ^a   Schneider, Benjamin J ^b   Ho, Christie C ^a   Nesteryuk, Vasyl ^a   Ngwesse, Stacy E ^b   Liu, Xianxian ^a   Parales, Juanito V ^a   Ditty, Jayna L ^b   Parales, Rebecca E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ST THOMAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CHEMOTAXIS; CHEMOTACTIC RESPONSE; DEGRADATION PATHWAYS; DIFFERENT MECHANISMS; ENVIRONMENTAL POLLUTANTS; GROWTH SUBSTRATES; PSEUDOMONAS PUTIDA F1; SIGNAL TRANSDUCTION SYSTEM;

BIOCHEMISTRY; BIODEGRADATION; BIOREMEDIATION; ESCHERICHIA COLI; GENES; PHYSIOLOGY; SIGNAL TRANSDUCTION; STYRENE;

METABOLISM;

CARRIER PROTEIN; PHENYLACETIC ACID; PHENYLACETIC ACID DERIVATIVE;

AROMATIC HYDROCARBON; BACTERIOLOGY; BACTERIUM; BIODEGRADATION; BIOREMEDIATION; BIOTECHNOLOGY; CATABOLISM; CHEMOTAXIS; GROWTH; MUTATION; ORGANIC POLLUTANT;

ARTICLE; CHEMOTAXIS; DRUG EFFECT; ESCHERICHIA COLI; GENETICS; METABOLISM; PHYSIOLOGY; PSEUDOMONAS PUTIDA; SIGNAL TRANSDUCTION;

CARRIER PROTEINS; CHEMOTAXIS; ESCHERICHIA COLI; PHENYLACETATES; PSEUDOMONAS PUTIDA; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PAA; PSEUDOMONAS PUTIDA;

EID: 84875493270     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03895-12     Document Type: Article

References (63)

1. Samanta SK, Singh OV, Jain RK. 2002. Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol. 20:243-248.
2. Haritash AK, Kaushik CP. 2009. Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J. Hazard. Mater. 169:1-15.
3. Luengo JM, García JL, Olivera ER. 2001. The phenylacetyl-CoA catabolon: a complex catabolic unit with broad biotechnological applications. Mol. Microbiol. 39:1434-1442.
4. Teufel A, Mascaraque V, Ismail W, Voss M, Perera J, Eisentreich W, Haehnel W, Fuchs G. 2010. Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proc. Natl. Acad. Sci. U. S. A. 107:14390-14395.
5. Wrightman F, Lighty DL. 1982. Identification of phenylacetic acid as a natural auxin in the shoots of higher plants. Physiol. Plant. 55:17-24.
6. Ismail W, El-Said Mohamed M, Wanner BL, Datsenko KA, Eisenreich W, Rohdich F, Bacher A, Fuchs G. 2003. Functional genomics by NMR spectroscopy. Phenylacetate catabolism in Escherichia coli. Eur. J. Biochem. 270:3047-3054.
7. Miñambres B, Martinez-Blanco H, Olivera ER, García B, Diez B, Barredo JL, Moreno MA, Schleissner C, Salto F, Luengo JM. 1996. Molecular cloning and expression in different microbes of the DNA encoding Pseudomonas putida U phenylacetyl-CoA ligase. J. Biol. Chem. 271:33531-33538.
8. Schleissner C, Olivera ER, Fernández-Valverde M, Luengo JM. 1994. Aerobic catabolism of phenylacetic acid in Pseudomonas putida U: biochemical characterization of a specific phenylacetic acid transport system and formal demonstration that phenylacetyl-coenzyme A is a catabolic intermediate. J. Bacteriol. 176:7667-7676.
9. Martínez-Blanco H, Reglero A, Rodriquez-Aparicio LB, Luengo JM. 1990. Purification and biochemical characterization of phenylacetyl-CoA ligase from Pseudomonas putida. J. Biol. Chem. 265:7084-7090.
10. Vitovski S. 1993. Phenylacetate-coenzyme A ligase is induced during growth on phenylacetic acid in different bacteria of several genera. FEMS Microbiol. Lett. 108:1-5.
11. Ferrández A, Miñambres B, García B, Olivera ER, Luengo JM, García JL, Díaz E. 1998. Catabolism of phenylacetic acid in Eschericia coli. J. Biol. Chem. 273:25974-25986.
12. Bartolomé-Martín D, Martínez-García E, Mascaraque V, Rubio J, Perera J, Alonso S. 2004. Characterization of a second functional gene cluster for the catabolism of phenylacetic acid in Pseudomonas sp. strain Y2. Gene 341:167-179.
13. Olivera ER, Miñambres B, García B, Muñiz C, Moreno MA, Ferrández A, Díaz E, García JL, Luengo JM. 1998. Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl- CoA catabolon. Proc. Natl. Acad. Sci. U. S. A. 95:6419-6424.
14. Parales RE, Ditty JL, Harwood CS. 2000. Toluene-degrading bacteria are chemotactic to the environmental pollutants benzene, toluene, and trichloroethylene. Appl. Environ. Microbiol. 66:4098-4104.
15. Hazelbauer GI, Falke JJ, Parkinson JS. 2008. Bacterial chemoreceptors; high-performance signalling in networked arrays. Trends Biochem. Sci. 33:9-19.
16. Alexandre G, Zhulin IB. 2001. More than one way to sense chemicals. J. Bacteriol. 183:4681-4686.
17. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
18. Law AM, Aitken MD. 2003. Bacterial chemotaxis to naphthalene desorbing from a nonaqueous liquid. Appl. Environ. Microbiol. 69:5968-5973.
19. Marx RB, Aitken MD. 2000. Bacterial chemotaxis enhances naphthalene degradation in a heterogeneous aqueous system. Environ. Sci. Technol. 34:3379-3383.
20. Pandey G, Jain RK. 2002. Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl. Environ. Microbiol. 68:5789-5795.
21. White AK, Metcalf WW. 2004. The htx and ptx operons of Pseudomonas stutzeri WM88 are new members of the Pho regulon. J. Bacteriol. 186: 5876-5882.
22. Figurski DH, Helinski DR. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Nat. Acad. Sci. U. S. A. 76:1648-1652.
23. Sambrook J, Fritch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Stanier RY, Palleroni NJ, Doudoroff M. 1966. The aerobic pseudomonad, a taxonomic study. J. Gen. Microbiol. 43:159-271.
25. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology (NY) 1:784-791.
26. Keen NT, Tamaki S, Kobayashi D, Trollinger D. 1988. Improved broadhost- range plasmids for DNA cloning in Gram-negative bacteria. Gene 70:191-197.
27. Sarand I, Osterberg S, Holmqvist S, Holmfeldt P, Skarfstad E, Parales RE, Shingler V. 2008. Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aerlike proteins of Pseudomonas putida. Environ. Microbiol. 10:1320-1334.
28. Adereth Y, Champion KJ, Hsu T, Dammai V. 2005. Site-directed mu-tagenesis using Pfu DNA polymerase and T4 DNA ligase. Biotechniques 38:864-868.
29. Parales RE, Harwood CS. 1993. Construction and use of a new broadhost- range lacZ transcriptional fusion vector, pHRP309, for Gram bacteria. Gene 133:23-30.
30. Harwood CS, Nichols NN, Kim MK, Ditty JL, Parales RE. 1994. Identification of the pcaRKF gene cluster from Pseudomonas putida: involvement in chemotaxis, biodegradation, and transport of 4-hydroxybenzoate. J. Bacteriol. 176:6479-6488.
31. Parkinson JS. 2007. A "bucket of light" for viewing bacterial colonies in soft agar. Methods Enzymol. 423:432-435.
32. Pham HT, Parkinson JS. 2011. Phenol sensing by Escherichia coli chemoreceptors: a nonclassical mechanism. J. Bacteriol. 193:6597-6604.
33. Storch KF, Rudolph J, Oesterhelt D. 1999. Car: a cytoplasmic sensor responsible for arginine chemotaxis in the archaeon Halobacterium salinarum. EMBO J. 18:1146-1158.
34. Miller JH. 1975. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
35. Song F, Zhuang Z, Finci L, Dunaway-Mariano D, Kniewel R, Bugliano JA, Solorzano V, Wu J, Lima CD. 2006. Structure, function, and mechanism of the phenylacetate pathway hog dog-fold thioesterase PaaI. J. Biol. Chem. 281:11028-11038.
36. Wadhams GH, Armitage JP. 2004. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5:1024-1037.
37. Liu X, Wood PL, Parales JV, Parales RE. 2009. Chemotaxis to pyrimidines and identification of a cytosine chemoreceptor in Pseudomonas putida. J. Bacteriol. 191:2909-2916.
38. Nichols NN, Harwood CS. 2000. An aerotaxis transducer gene from Pseudomonas putida. FEMS Microbiol. Lett. 182:177-183.
39. Taylor BL, Watts KJ, Johnson MS. 2007. Oxygen and redox sensing by two-component systems that regulate behavioral responses: behavioral assays and structural studies of aer using in vivo disulfide cross-linking. Methods Enzymol. 422:190-232.
40. Liu X. 2009. Chemotaxis to pyrimidines and s-triazines in Pseudomonas and Escherichia coli. Ph.D. dissertation. University of California, Davis, Davis, CA.
41. Parkinson JS, Houts SE. 1982. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J. Bacteriol. 151
42. Bibikov SI, Biran R, Rudd KE, Parkinson JS. 1997. A signal transducer for aerotaxis in Escherichia coli. J. Bacteriol. 179:4075-4079.
43. Rebbapragada A, Johnson MS, Harding GP, Zuccarelli AJ, Fletcher HM, Zhulin IB, Taylor BL. 1997. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc. Natl. Acad. Sci. U. S. A. 94:10541-10546.
44. Alexandre G, Greer-Phillips S, Zhulin IB. 2004. Ecological role of energy taxis in microorganisms. FEMS Microbiol. Rev. 28:113-126.
45. Taylor BL. 2007. Aer on the inside looking out: paradigm for a PASHAMP role in sensing oxygen, redox and energy. Mol. Microbiol. 65: 1415-1424.
46. Repik A, Rebbapragada A, Johnson MS, Haznedar JÖ, Zhulin IB, Taylor BL. 2000. PAS domain residues involved in signal transduction by the Aer redox sensor of Escherichia coli. Mol. Microbiol. 36:806-816.
47. Schweinitzer T, Josenhans C. 2010. Bacterial energy taxis: a global strategy? Arch. Microbiol. 192:507-520.
48. Alexandre G. 2010. Coupling metabolism and chemotaxis-dependent behaviours by energy taxis receptors. Microbiology 156:2283-2293.
49. Rabinovitch-Deere CA, Parales RE. 2012. Three types of taxis used in the response of Acidovorax sp. strain JS42 to 2-nitrotoluene. Appl. Environ. Microbiol. 78:2308-2315.
50. Grimm AC, Harwood CS. 1999. NahY, a catabolic plasmid-encoded receptor required for chemotaxis of Pseudomonas putida to the aromatic hydrocarbon naphthalene. J. Bacteriol. 181:3310-3316.
51. Iwaki H, Muraki T, Ishihara S, Hasegawa Y, Rankin KN, Sulea T, Boyd J, Lau PCK. 2007. Characterization of a pseudomonad 2-nitrobenzoate nitroreductase and its catabolic pathway-associated 2-hydroxylaminobenzoate mutase and a chemoreceptor involved in 2-nitrobenzoate chemotaxis. J. Bacteriol. 189:3502-3514.
52. Lacal J, Muñoz-Martínez F, Reyes-Darías JA, Duque E, Matilla M, Segura A, Calvo JJ, Jímenez-Sánchez C, Krell T, Ramos JL. 2011. Bacterial chemotaxis towards aromatic hydrocarbons in Pseudomonas. Environ. Microbiol. 13:1733-1744.
53. Ditty JL, Harwood CS. 1999. Conserved cytoplasmic loops are important for both the transport and chemotaxis functions of PcaK, a protein from Pseudomonas putida with 12 membrane-spanning regions. J. Bacteriol. 181:5068-5074.
54. Ditty JL, Harwood CS. 2002. Charged amino acids conserved in the aromatic acid/H symporter family of permeases are required for 4-hydroxybenzoate transport by PcaK from Pseudomonas putida. J. Bacteriol. 184:1444-1448.
55. Nichols NN, Harwood CS. 1997. PcaK, a high-affinity permease for the aromatic compounds 4-hydroxybenzoate and protocatechuate from Pseudomonas putida. J. Bacteriol. 179:5056-5061.
56. Hawkins AC, Harwood CS. 2002. Chemotaxis of Ralstonia eutropha JMP134(pJP4) to the herbicide 2,4-dichlorophenoxyacetate. Appl. Environ. Microbiol. 68:968-972.
57. Beltrametti F, Marconi AM, Bestetti G, Colombo C, Galli E, Ruzzi M, Zennaro E. 1997. Sequencing and functional analysis of styrene catabolism genes from Pseudomonas fluorescens ST. Appl. Environ. Microbiol. 63:2232-2239.
58. O'Conner K, Buckley CM, Hartmans S, Dobson ADW. 1995. Possible regulatory role for nonaromatic carbon sources in styrene degradation by Pseudomonas putida CA-3. Appl. Environ. Microbiol. 61:544-548.
59. O'Leary ND, O'Conner KE, Duetz W, Dobson ADW. 2001. Transcriptional regulation of styrene degradation in Pseudomonas putida CA-3. Microbiology 147:973-979.
60. Velasco A, Alonso S, García JL, Perera J, Díaz E. 1998. Genetic and functional analysis of the styrene catabolic cluster of Pseudomonas sp. strain Y2. J. Bacteriol. 180:1063-1071.
61. Finette BA, Subramanian V, Gibson DT. 1984. Isolation and characterization of Pseudomonas putida PpF1 mutants defective in the toluene dioxygenase enzyme system. J. Bacteriol. 160:1003-1009.
62. Gibson DT, Hensley M, Yoshioka H, Mabry TJ. 1970. Formation of ()-cis-2,3-dihydroxy-1-methylcyclohexa-4,6-diene from toluene by Pseudomonas putida. Biochemistry 9:1626-1630.
63. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.