Catabolic pathways and cellular responses of Pseudomonas putida P8 during growth on benzoate with a proteomics approach

Biotechnology and Bioengineering

Volumn 101, Issue 6, 2008, Pages 1297-1312

  Cao, Bin ^a   Loh, Kai Chee ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

2 DE; Benzoate biodegradation; MALDI TOF MS; meta cleavage pathway; ortho cleavage pathway; Pseudomonas putida P8

Indexed keywords

AMINES; BINDING ENERGY; BIOCHEMISTRY; BIODEGRADATION; CARBOHYDRATES; CATALYSTS; CELL PROLIFERATION; COLLOIDS; CONCENTRATION (PROCESS); DEGRADATION; DESORPTION; DETOXIFICATION; DIGITAL ARITHMETIC; ELECTROPHORESIS; ENZYMES; GELATION; GELS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; MOLECULAR BIOLOGY; NUCLEIC ACIDS; ORGANIC ACIDS; ORGANIC COMPOUNDS; PHYSIOLOGICAL MODELS; SEARCH ENGINES; TWO DIMENSIONAL;

2-DE; BENZOATE BIODEGRADATION; MALDI-TOF MS; META-CLEAVAGE PATHWAY; ORTHO-CLEAVAGE PATHWAY; PSEUDOMONAS PUTIDA P8;

PROTEINS;

ABC TRANSPORTER; BENZOIC ACID; CATECHOL 1,2 DIOXYGENASE; CATECHOL 2,3 DIOXYGENASE; DNA BINDING PROTEIN; ISOCITRATE DEHYDROGENASE;

ARTICLE; BACTERIAL GROWTH; CATABOLISM; ENZYME ACTIVITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROBIAL DEGRADATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DETERMINATION; PROTEOMICS; PSEUDOMONAS PUTIDA; UNINDEXED SEQUENCE;

BACTERIAL PROTEINS; BENZOATES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; METABOLIC NETWORKS AND PATHWAYS; PROTEOME; PSEUDOMONAS PUTIDA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ARCA; BACTERIA (MICROORGANISMS); PSEUDOMONAS PUTIDA;

EID: 54349090860     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.21997     Document Type: Article

References (76)

1. Ahamad PYA, Kunhi AAM. 1996. Degradation of phenol through ortho-cleavage pathway by Pseudomonas stutzeri strain SPC2. Lett Appl Microbiol 22(1):26-29.
2. Alexander M. 1981. Biodegradation of chemicals of environmental concern. Science 211(4478):132-138.
3. Altenschmidt U, Oswald B, Fuchs G. 1991. Purification and characterization of benzoate-Coenzyme-A ligase and 2-aminobenzoate-Coenzyme-A ligases from a denitrifying Pseudomonas sp. J Bacteriol 173(17):5494-5501.
4. Altenschmidt U, Oswald B, Steiner E, Herrmann H, Fuchs G. 1993. New aerobic benzoate oxidation pathway via benzoyl-Coenzyme-A and 3-hydroxybenzoyl-Coenzyme-A in a denitrifying Pseudomonas sp. J Bacteriol 175(15):4851-4858.
5. Ampe F, Lindley ND. 1996. Flux limitations in the ortho pathway of benzoate degradation of Alcaligenes eutrophus: Metabolite overflow and induction of the meta pathway at high substrate concentrations. Microbiology 142:1807-1817.
6. Benndorf D, Thiersch M, Loffhagen N, Kunath C, Harms H. 2006. Pseudomonas putida KT2440 responds specifically to chlorophenoxy herbicides and their initial metabolites. Proteomics 6(11):3319-3329.
7. Bhushan B, Halasz A, Hawari M. 2005. Biotransformation of CL-20 by a dehydrogenase enzyme from Clostridium sp EDB2. Appl Microbiol Biotechnol 69(4):448-455.
8. Bouwer EJ, Zehnder AJB. 1993. Bioremediation of organic compounds - Putting microbial metabolism to work. Trends Biotechnol 11(8):360-367.
9. Callewaert DM, Rosemblatt MS, Suzuki K, Tchen T. 1973. Succinc semialdehyde dehydrogenase from a Pseudomonas species. I. Purification and chemical properties. J Biol Chem 248(17):6009-6013.
10. Cowles CE, Nichols NN, Harwood CS. 2000. BenR, a XylS homologue, regulates three different pathways of aromatic acid degradation in Pseudomonas putida. J Bacteriol 182(22):6339-6346.
11. Denef VJ, Patrauchan MA, Florizone C, Park J, Tsoi TV, Verstraete W, Tiedje JM, Eltis LD. 2005. Growth substrate- and phase-specific expression of biphenyl, benzoate, and C-1 metabolic pathways in Burkholderia xenovorans LB400. J Bacteriol 187(23):7996-8005.
12. Dominguez-Cuevas P, Gonzalez-Pastor JE, Marques S, Ramos JL, de Lorenzo V. 2006. Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J Biol Chem 281(17):11981-11991.
13. Dua M, Singh A, Sethunathan N, Johri AK. 2002. Biotechnology and bioremediation: Successes and limitations. Appl Microbiol Biotechnol 59(2-3):143-152.
14. Fridovich I. 1978. The biology of oxygen radicals. Science 201:875-880.
15. Galvao TC, de Lorenzo V. 2006. Transcriptional regulators a la carte: Engineering new effector specificities in bacterial regulatory proteins. Curr Opin Biotechnol 17(1):34-42.
16. Ganoza MC, Aoki H. 2000. Peptide bond synthesis: Function of the efp gene product. Biol Chem 381(7):553-559.
17. Greated A, Lambertsen L, Williams PA, Thomas CM. 2002. Complete sequence of the IncP-9 TOL plasmid pWW0 from Pseudomonas putida. Environ Microbiol 4(12):856-871.
18. Hamzah RY, Albaharna BS. 1994. Catechol ring-cleavage in Pseudomonas cepacia - the simultaneous induction of ortho and meta pathways. Appl Microbiol Biotechnol 41(2):250-256.
19. Harayama S, Rekik M. 1990. The meta-cleavage operon of TOL degradative plasmid pWW0 comprises 13 genes. Mol Gen Genet 221(1):113-120.
20. Hartig C, Loffhagen N, Harms H. 2005. Formation of trans fatty acids is not involved in growth-linked membrane adaptation of Pseudomonas putida. Appl Environ Microbiol 71(4):1915-1922.
21. Harwood CS, Parales RE. 1996. The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:553-590.
22. 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(21):6479-6488.
23. Hassett DJ, Schweizer HP, Ohman DE. 1995. Pseudomonas aeruginosa SodA and SodB mutants defective in manganese-cofactored and iron-cofactored superoxide-dismutase activity demonstrate the importance of the iron-cofactored form in aerobic metabolism. J Bacteriol 177(22): 6330-6337.
24. Heim S, Ferrer M, Heuer H, Regenhardt D, Nimtz M, Timmis KN. 2003. Proteome reference map of Pseudomonas putida strain KT2440 for genome expression profiling: Distinct responses of KT2440 and Pseudomonas aeruginosa strain PAO1 to iron deprivation and a new form of superoxide dismutase. Environ Microbiol 5(12):1257-1269.
25. Heipieper HJ, Diefenbach R, Keweloh H. 1992. Conversion of cis unsaturated fatty-acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol 58(6):1847-1852.
26. Hishinuma S, Yuki M, Fujimura M, Fukumori F. 2006. OxyR regulated the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida. Environ Microbiol 8(12):2115-2124.
27. Holtwick R, Keweloh H, Meinhardt F. 1999. Cis/trans isomerase of unsaturated fatty acids of Pseudomonas putida P8: Evidence for a heme protein of the cytochrome C type. Appl Environ Microbiol 65(6):2644-2649.
28. Holtwick R, von Wallbrunn A, Keweloh H, Meinhardt F. 2001. A novel rolling-circle-replicating plasmid from Pseudomonas putida P8: Molecular characterization and use as vector. Microbiology 147:337-344.
29. Inouye S, Nkazawa A, Nkazawa T. 1981. Molecular cloning of gene xylS of the TOL plasmid evidence for positive regulation of the xylDEGF operon by xylS. J Bacteriol 148:413-418.
30. Iwaki H, Hasegawa Y. 2007. Degradation of 2-nitrobenzoate by Burkholderia terrae strain KU-15. Biosci Biotechnol Biochem 71(1):145-151.
31. Jimenez JI, Minambres B, Garcia JL, Diaz E. 2002. Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4(12):824-841.
32. Kasak L, Horak R, Nurk A, Talvik K, Kivisaar M. 1993. Regulation of the catechol 1,2-dioxygenase-encoding and phenol monooxygenase-encoding pheBA Operon in Pseudomonas putida PAW85. J Bacteriol 175(24):8038-8042.
33. Kim SI, Kim SJ, Nam MH, Kim SH, Ha KS, Oh KH, Yoo JS, Park YM. 2002. Proteome analysis of aniline-induced proteins in Acinetobacter lwoffii K24. Curr Microbiol 44(1):61-66.
34. Kim SI, Song SY, Kim KW, Ho EM, Oh KH. 2003. Proteomic analysis of the benzoate degradation pathway in Acinetobacter sp KS-1. Res Microbiol 154(10):697-703.
35. Kim SI, Kim JY, Yun SH, Kim JH, Leem SH, Lee C. 2004. Proteome analysis of Pseudomonas sp K82 biodegradation pathways. Proteomics 4(11):3610-3621.
36. Kim YH, Cho K, Yun S-H, Kim JY, Kwon K-H, Yoo JS, Kim SI. 2006. Analysis of aromatic catabolic pathways in Pseudomonas putida KT 2440 using a combined proteomic approach: 2-DE/MS and cleavable isotope-coded affinity tag analysis. Proteomics 6(4):1301-1318.
37. Krayl M, Benndorf D, Loffhagen N, Babel W. 2003. Use of proteomics and physiological characteristics to elucidate ecotoxic effects of methyl tert-butyl ether in Pseudomonas putida KT2440. Proteomics 3(8):1544-1552.
38. Krishnan S, Prabhu Y, Phale PS. 2004. O-phthalic acid, a dead-end product in one of the two pathways of phenanthrene degradation in Pseudomonas sp strain PP2. Indian J Biochem Biophys 41(5):227-232.
39. Kurbatov L, Albrecht D, Herrmann H, Petruschka L. 2006. Analysis of the proteome of Pseudomonas putida KT2440 grown on different sources of carbon and energy. Environ Microbiol 8(3):466-478.
40. Lau PCK, Wang Y, Patel A, Labbe D, Bergeron H, Brousseau R, Konishi Y, Rawlings M. 1997. A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc Natl Acad Sci USA 94(4):1453-1458.
41. Lee N, Lee JM, Min KH, Kwon DY. 2003. Purification and characterization of 2,3-dihydroxybiphenyl 1,2-dioxygenase from Comamonas sp SMN4. J Microbiol Biotechnol 13(4):487-494.
42. Loh KC, Chua SS. 2002. Ortho pathway of benzoate degradation in Pseudomonas putida: Induction of meta pathway at high substrate concentrations. Enzyme Microb Technol 30(5):620-626.
43. Loh KC, Wu TT. 2006. Cometabolic transformation of 2-chlorophenol and 4-chlorophenol in the presence of phenol by Pseudomonas putida. Can J Chem Eng 84(3):356-367.
44. Martinez A, Kolter R. 1997. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179(16):5188-5194.
45. Molina-Henares AJ, Krell T, Guazzaroni ME, Segura A, Ramos JL. 2006. Members of the IclR family of bacterial transcriptional regulators function as activators and/or repressors. FEMS Microbiol Rev 30(2):157-186.
46. Mosqueda G, Ramos-Gonzalez MI, Ramos JL. 1999. Toluene metabolism by the solvent-tolerant Pseudomonas putida DOT-T1 strain, and its role in solvent impermeabilization. Gene 232(1):69-76.
47. Nair S, Finkel SE. 2004. Dps protects cells against multiple stresses during stationary phase. J Bacteriol 186(13):4192-4198.
48. Nakazawa T, Nakazawa A. 1970. Pyrocatechase (Pseudomonas). Methods Enzymol 17A:518-522.
49. Nichols NN, Harwood CS. 1995. Repression of 4-hydroxybenzoate transport and degradation by benzoate - A new layer of regulatory control in the Pseudomonas putida beta-ketoadipate pathway. J Bacteriol 177(24):7033-7040.
50. Nivens DE, McKnight TE, Moser SA, Osbourn SJ, Simpson ML, Sayler GS. 2004. Bioluminescent bioreporter integrated circuits: Potentially small, rugged and inexpensive whole-cell biosensors for remote environmental monitoring. J Appl Microbiol 96(1):33-46.
51. Nozaki M. 1970. Metapyrocatechase (Pseudomonas). Methods Enzymol 17A:522-525.
52. Parales RE. 2004. Nitrobenzoates and aminobenzoates are chemoattractants for Pseudomonas strains. Appl Environ Microbiol 70(1):285-292.
53. Parales RE, Haddock JD. 2004. Biocatalytic degradation of pollutants. Curr Opin Biotechnol 15(4):374-379.
54. Parales RE, Bruce NC, Schmid A, Wackett LP. 2002. Biodegradation, biotransformation, and biocatalysis (B3). Appl Environ Microbiol 68(10):4699-4709.
55. Park HS, Kim HS. 2001. Genetic and structural organization of the aminophenol catabolic operon and its implication for evolutionary process. J Bacteriol 183:5074-5081.
56. Patrauchan MA, Florizone C, Dosanjh M, Molm WW, Davies J, Eltis LD. 2005. Catabolism of benzoate and phthalate in Rhodococcus sp strain RH A1: Redundancies and convergence. J Bacteriol 187(12):4050-4063.
57. Prabhu Y, Phale PS. 2003. Biodegradation of phenanthrene by Psuedomonas sp strain P P2: Novel metabolic pathway, role of biosurfactant and cell surface hydrophobicity in hydrocarbon assimilation. Appl Microbiol Biotechnol 61(4):342-351.
58. Ramos JL, Marques S, Timmis KN. 1997. Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators. Annu Rev Microbiol 51:341-373.
59. Raskin DM, deBoer PAJ. 1997. The MinE ring: An FtsZ-independent cell structure required for selection of the correct division site in E-coli. Cell 91(5):685-694.
60. Romero-Steiner S, Parales RE, Harwood CS, Houghton JE. 1994. Characterization of the pcaR regulatory gene from Pseudomonas putida, which is required for the complete degradation of p-hydroxybenzoate. J Bacteriol 176:5771-5779.
61. Rothmel RK, Aldrich TL, Houghton JE, Coco WM, Ornston LN, Chakrabarty AM. 1990. Nucleotide sequencing and characterization of Pseudomonas putida CatR-A positive regulator of the CatBC operon is a member of the LysR family. J Bacteriol 172(2):922-931.
62. Santos PM, Benndorf D, Sa-Correia I. 2004. Insights into Pseudomonas putida KT2440 response to phenol-induced stress by quantitative proteomics. Proteomics 4:2640-2652.
63. Segura A, Godoy P, van Dillewijn P, Hurtado A, Arroyo N, Santacruz S, Ramos JL. 2005. Proteomic analysis reveals the participation of energy-and stress-related proteins in the response of Pseudomonas putida DOT-T1E to toluene. J Bacteriol 187(17):5937-5945.
64. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 68(5):850-858.
65. Shingler V, Moore T. 1994. Sensing of aromatic-compounds by the DmpR transcriptional activator of phenol-catabolizing Pseudomonas sp strain CF600. J Bacteriol 176(6):1555-1560.
66. Shingler V, Bartilson M, Moore T. 1993. Cloning and nucleotide-sequence of the gene encoding the positive regulator (DmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators. J Bacteriol 175(6):1596-1604.
67. Sondossi M, Sylvestre M, Ahmad D. 1992. Effects of chlorobenzoate transformation on the Pseudomonas testosteroni biphenyl and chlorobiphenyl degradation pathway. Appl Environ Microbiol 58(2):485-495.
68. Sticher P, Jaspers MCM, Stemmler K, Harms H, Zehnder AJB, vanderMeer JR. 1997. Development and characterization of a whole-cell bioluminescent sensor for bioavailable middle-chain alkanes in contaminated groundwater samples. Appl Environ Microbiol 63(10):4053-4060.
69. Tomas-Gallardo L, Ganosa I, Santero E, Camafeita E, Calvo E, Lopez JA, Floriano B. 2006. Proteomic and transcriptional characterization of aromatic degradation pathways in Rhodoccocus sp. strain TFB. Proteomics 6(S1):S119-S132.
70. Trogl J, Ripp S, Kuncova G, Sayler GS, Churava A, Parik P, Demnerova K, Halova J, Kubicova L. 2005. Selectivity of whole cell optical biosensor with immobilized bioreporter Pseudomonas fluorescens HK44. Sens Actuator B Chem 107(1):98-103.
71. Tropel D, van der Meer JR. 2004. Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Micriobiol Mol Biol Rev 68(3):474-500.
72. Tsirogianni I, Aivaliotis M, Karas M, Tsiotis G. 2004. Mass spectrometric mapping of the enzymes involved in the phenol degradation of an indigenous soil pseudomonad. Biochim Biophys Acta Proteins Proteomics 1700(1):117-123.
73. Tsirogianni E, Aivaliotis M, Papasotiriou DG, Karas M, Tsiotis G. 2006. Identification of inducible protein complexes in the phenol degrader Pseudomonas sp strain phDV1 by blue native gel electrophoresis and mass spectrometry. Amino Acids 30(1):63-72.
74. Wang SJ, Loh KC. 2000. New cell growth pattern on mixed substrates and substrate utilization in cometabolic transformation of 4-chlorophenol. Water Res 34(15):3786-3794.
75. Wang SJ, Loh KC, Chua SS. 2003. Prediction of critical cell growth behavior of Pseudomonas putida to maximize the cometabolism of 4-chlorophenol with phenol and sodium glutamate as carbon sources. Enzyme Microb Technol 32(3-4):422-430.
76. Yun S-H, Kim YH, Joo EJ, Choi J-S, Sohn J-H, Kim SI. 2006. Proteome analysis of cellular response of Pseudomonas putida KT2440 to tetracycline stress. Curr Microbiol 53(2):95-101.