The polyhydroxyalkanoate metabolism controls carbon and energy spillage in Pseudomonas putida

Environmental Microbiology

Volumn 14, Issue 4, 2012, Pages 1049-1063

  Escapa, I F ^a   Garcia J L ^a   Buhler B ^b   Blank, L M ^b   Prieto, M A ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b TU DORTMUND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; CARBON; GLYOXYLIC ACID DERIVATIVE; NITROGEN; POLYHYDROXYALKANOIC ACID;

ARTICLE; BIOREMEDIATION; CITRIC ACID CYCLE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PSEUDOMONAS PUTIDA;

ACETYL COENZYME A; BIODEGRADATION, ENVIRONMENTAL; CARBON; CITRIC ACID CYCLE; GLYOXYLATES; NITROGEN; POLYHYDROXYALKANOATES; PSEUDOMONAS PUTIDA;

BACTERIA (MICROORGANISMS); PSEUDOMONAS PUTIDA;

EID: 84859432691     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02684.x     Document Type: Article

References (85)

1. Babel, W. (1992) Pecularities of methylotrophs concerning overflow metabolism, especially the synthesis of polyhydroxyalkanoates. FEMS Microbiol Lett 103: 141-148.
2. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 57: 289-300.
3. Bertani, G. (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186: 595-600.
4. Blank, L.M., and Kuepfer, L. (2010) Metabolic flux distributions: genetic information, computational predictions, and experimental validation. Appl Microbiol Biotechnol 86: 1243-1255.
5. Blank, L.M., Ebert, B.E., Bühler, B., and Schmid, A. (2008) Metabolic capacity estimation of Escherichia coli as a platform for redox biocatalysis: constraint-based modeling and experimental verification. Biotechnol Bioeng 100: 1050-1065.
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
7. Brigham, C.J., Budde, C.F., Holder, J.W., Zeng, Q., Mahan, A.E., Rha, C., and Sinskey, A.J. (2010) Elucidation of beta-oxidation pathways in Ralstonia eutropha H16 by examination of global gene expression. J Bacteriol 192: 5454-5464.
8. Budde, C.F., Mahan, A.E., Lu, J., Rha, C., and Sinskey, A.J. (2010) Roles of multiple acetoacetyl coenzyme A reductases in polyhydroxybutyrate biosynthesis in Ralstonia eutropha H16. J Bacteriol 192: 5319-5328.
9. Campbell, C.D., Chapman, S.J., Cameron, C.M., Davidson, M.S., and Potts, J.M. (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69: 3593-3599.
10. Chen, G.Q. (2009) A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem Soc Rev 38: 2434-2446.
11. Dawes, E.A. (1986) Microbial Energetics. Glasgow, UK: Blackie and Son.
12. Domínguez-Cuevas, P., González-Pastor, J.-E., Marqués, S., Ramos, J.-L., and de Lorenzo, V. (2006) Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J Biol Chem 281: 11981-11991.
13. Emmerling, M., Dauner, M., Ponti, A., Fiaux, J., Hochuli, M., Szyperski, T., etal. (2002) Metabolic flux responses to pyruvate kinase knockout in Escherichia coli. J Bacteriol 184: 152-164.
14. Escapa, I.F., Morales, V., Martino, V.P., Pollet, E., Averous, L., García, J.L., and Prieto, M.A. (2011) Disruption of beta-oxidation pathway in Pseudomonas putida KT2442 to produce new functionalized PHAs with thioester groups. Appl Microbiol Biotechnol 89: 1583-1598.
15. de Eugenio, L.I., Galán, B., Escapa, I.F., Maestro, B., Sanz, J.M., García, J.L., and Prieto, M.A. (2010a) The PhaD regulator controls the simultaneous expression of the pha genes involved in polyhydroxyalkanoate metabolism and turnover in Pseudomonas putida KT2442. Environ Microbiol 12: 1591-1603.
16. de Eugenio, L.I., Escapa, I.F., Morales, V., Dinjaski, N., Galán, B., García, J.L., and Prieto, M.A. (2010b) The turnover of medium-chain-length polyhydroxyalkanoates in Pseudomonas putida KT2442 and the fundamental role of PhaZ depolymerase for the metabolic balance. Environ Microbiol 12: 207-221.
17. Fischer, E., and Sauer, U. (2003) Metabolic flux profiling of Escherichia coli mutants in central carbon metabolism using GC-MS. Eur J Biochem 270: 880-891.
18. Fuhrer, T., Fischer, E., and Sauer, U. (2005) Experimental identification and quantification of glucose metabolism in seven bacterial species. J Bacteriol 187: 1581-1590.
19. Galán, B., Kolb, A., García, J.L., and Prieto, M.A. (2001) Superimposed levels of regulation of the 4-hydroxyphenylacetate catabolic pathway in Escherichia coli. J Biol Chem 276: 37060-37068.
20. Galán, B., Dinjaski, N., Maestro, B., de Eugenio, L.I., Escapa, I.F., Sanz, J.M., etal. (2011) Nucleoid-associated PhaF phasin drives intracellular location and segregation of polyhydroxyalkanoate granules in Pseudomonas putida KT2442. Mol Microbiol 79: 402-418.
21. Goldberg, D.M., and Ellis, G. (1983) Isocitrate dehydrogenase. In Methods of Enzymatic Analysis. Bergmeyer, H.U., Bergmeyer, J., and Grasse, M. (eds). Weinheim, Germany: Verlag Chemie, pp. 183-190.
22. Haywood, G.W., Anderson, A.J., Chu, L., and Dawes, E.A. (1988) The role of NADH- and NADPH-linked acetoacetyl-CoA reductases in the poly-3-hydroxybutyrate synthesizing organism Alcaligenes eutrophus. FEMS Microbiol Lett 52: 259-264.
23. Herrero, M., de Lorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557-6567.
24. Hervás, A.B., Canosa, I., and Santero, E. (2008) Transcriptome analysis of Pseudomonas putida in response to nitrogen availability. J Bacteriol 190: 416-420.
25. Hervás, A.B., Canosa, I., Little, R., Dixon, R., and Santero, E. (2009) NtrC-dependent regulatory network for nitrogen assimilation in Pseudomonas putida. J Bacteriol 191: 6123-6135.
26. Hervás, A.B., Canosa, I., and Santero, E. (2010) Regulation of glutamate dehydrogenase expression in Pseudomonas putida results from its direct repression by NtrC under nitrogen-limiting conditions. Mol Microbiol 78: 305-319.
27. Heyland, J., Fu, J., and Blank, L.M. (2009) Correlation between TCA cycle flux and glucose uptake rate during respiro-fermentative growth of Saccharomyces cerevisiae. Microbiology 155: 3827-3383.
28. Hoffmann, N., and Rehm, B.H.A. (2004) Regulation of polyhydroxyalkanoate biosynthesis in Pseudomonas putida and Pseudomonas aeruginosa. FEMS Microbiol Lett 237: 1-7.
29. Hoffmann, N., and Rehm, B.H.A. (2005) Nitrogen-dependent regulation of medium-chain length polyhydroxyalkanoate biosynthesis genes in pseudomonads. Biotechnol Lett 27: 279-282.
30. Jenkins, L.S., and Nunn, W.D. (1987) Genetic and molecular characterization of the genes involved in short-chain fatty acid degradation in Escherichia coli: the ato system. J Bacteriol 169: 42-52.
31. Jishage, M., Iwata, A., Ueda, S., and Ishihama, A. (1996) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J Bacteriol 178: 5447-5451.
32. Kabir, M., and Shimizu, K. (2003) Gene expression patterns for metabolic pathway in pgi knockout Escherichia coli with and without phb genes based on RT-PCR. J Biotechnol 105: 11-31.
33. Katsuki, H., Yoshida, T., Tanegashima, C., and Tanaka, S. (1971) Improved direct method for determination of keto acids by 2, 4-dinitrophenylhydrazine. Anal Biochem 43: 349-356.
34. Kessler, B., and Witholt, B. (2001) Factors involved in the regulatory network of polyhydroxyalkanoate metabolism. J Biotechnol 86: 97-104.
35. Klinke, S., Dauner, M., Scott, G., Kessler, B., and Witholt, B. (2000) Inactivation of isocitrate lyase leads to increased production of medium-chain-length poly(3-hydroxyalkanoates) in Pseudomonas putida. Appl Environ Microbiol 66: 909-913.
36. Lageveen, R.G., Huisman, G.W., Preusting, H., Ketelaar, P., Eggink, G., and Witholt, B. (1988) Formation of polyesters by Pseudomonas oleovorans: effect of substrates on formation and composition of poly-(R)-3-hydroxyalkanoates and poly-(R)-3-hydroxyalkenoates. Appl Environ Microbiol 54: 2924-2932.
37. Lee, I.Y., Kim, M.K., Park, Y.H., and Lee, S.Y. (1996) Regulatory effects of cellular nicotinamide nucleotides and enzyme activities on poly(3-hydroxybutyrate) synthesis in recombinant Escherichia coli. Biotechnol Bioeng 52: 707-712.
38. Lenz, R.W., Kim, Y.B., and Fuller, R.C. (1992) Production of unusual bacterial polyesters by Pseudomonas oleovorans through cometabolism. FEMS Microbiol Lett 103: 207-214.
39. Li, W., and Lu, C.D. (2007) Regulation of carbon and nitrogen utilization by CbrAB and NtrBC two-component systems in Pseudomonas aeruginosa. J Bacteriol 189: 5413-5420.
40. Li, Z.-J., Cai, L., Wu, Q., and Chen, G.-Q. (2009) Overexpression of NAD kinase in recombinant Escherichia coli harboring the phbCAB operon improves poly(3-hydroxybutyrate) production. Appl Microbiol Biotechnol 83: 939-947.
41. de Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172: 6568-6572.
42. Luengo, J.M., García, B., Sandoval, A., Naharro, G., and Olivera, E.R. (2003) Bioplastics from microorganisms. Curr Opin Microbiol 6: 251-260.
43. Madison, L.L., and Huisman, G.W. (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63: 21-53.
44. Moldes, C., García, P., García, J.L., and Prieto, M.A. (2004) In vivo immobilization of fusion proteins on bioplastics by the novel tag BioF. Appl Environ Microbiol 70: 3205-3212.
45. Morales, G., Ugidos, A., and Rojo, F. (2006) Inactivation of the Pseudomonas putida cytochrome o ubiquinol oxidase leads to a significant change in the transcriptome and to increased expression of the CIO and cbb3-1 terminal oxidases. Environ Microbiol 8: 1764-1774.
46. Nelson, K.E., Weinel, C., Paulsen, I.T., Dodson, R.J., Hilbert, H., Martins dos Santos, V.A., etal. (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4: 799-808.
47. Nikodinovic-Runic, J., Flanagan, M., Hume, A.R., Cagney, G., and O'Connor, K.E. (2009) Analysis of the Pseudomonas putida CA-3 proteome during growth on styrene under nitrogen-limiting and non-limiting conditions. Microbiology 155: 3348-3361.
48. Ninfa, A.J., and Jiang, P. (2005) PII signal transduction proteins: sensors of a-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8: 168-173.
49. Nogales, J., Palsson, B.O., and Thiele, I. (2008) A genome-scale metabolic reconstruction of Pseudomonas putida KT2440: iJN746 as a cell factory. BMC Syst Biol 2: 79.
50. Peoples, O.P., and Sinskey, A.J. (1989) Poly-b-hydroxybutyrate (PHB) biosynthesis in Alcaligenes eutrophus H16. Identification and characterization of the PHB polymerase gene (phbC). J Biol Chem 264: 15298-15303.
51. Peplinski, K., Ehrenreich, A., Doring, C., Bomeke, M., Reinecke, F., Hutmacher, C., and Steinbuchel, A. (2010) Genome-wide transcriptome analyses of the 'Knallgas' bacterium Ralstonia eutropha H16 with regard to polyhy-droxyalkanoate metabolism. Microbiology 156: 2136-2152.
52. Prieto, M.A., de Eugenio, L.I., Galán, B., Luengo, J.M., and Witholt, B. (2007) Synthesis and degradation of polyhydroxyalkanoates. In Pseudomonas: A Model System in Biology. Ramos, J.L., and Filloux, A. (eds). Berlin, Germany: Springer, pp. 397-428.
53. Puchalka, J., Oberhardt, M.A., Godinho, M., Bielecka, A., Regenhardt, D., Timmis, K.N., etal. (2008) Genome-scale reconstruction and analysis of the Pseudomonas putida KT2440 metabolic network facilitates applications in biotechnology. PLoS Comput Biol 4: e1000210.
54. Raberg, M., Peplinski, K., Heiss, S., Ehrenreich, A., Voigt, B., Doring, C., etal. (2011) Proteomic and transcriptomic elucidation of the mutant Ralstonia eutropha G+1 with regard to glucose utilization. Appl Environ Microbiol 77: 2058-2070.
55. Ramalingam, S., Vikram, M., Vigneshbabu, M.P., and Sivasankari, M. (2011) Flux balance analysis for maximizing polyhydroxyalkanoate production in Pseudomonas putida. Indian J Biotechnol 10: 70-74.
56. Rehm, B.H. (2010) Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 8: 578-592.
57. Riley, M. (1993) Functions of the gene products of Escherichia coli. Microbiol Mol Biol Rev 57: 862-952.
58. Rojo, F. (2010) Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 34: 658-684.
59. Romanov, V., Merski, M.T., and Hausinger, R.P. (1999) Assays for allantoinase. Anal Biochem 268: 49-53.
60. 2 measurement in soils. Soil Biol Biochem 27: 373-375.
61. Russell, J.B. (2007) The energy spilling reactions of bacteria and other organisms. J Mol Microbiol Biotechnol 13: 1-11.
62. Ruth, K., de Roo, G., Egli, T., and Ren, Q. (2008) Identification of two acyl-CoA synthetases from Pseudomonas putida GPo1: one is located at the surface of polyhydroxyalkanoates granules. Biomacromolecules 9: 1652-1659.
63. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
64. Sánchez, A.M., Andrews, J., Hussein, I., Bennett, G.N., and San, K.Y. (2006) Effect of overexpression of a soluble pyridine nucleotide transhydrogenase (UdhA) on the production of poly(3-hydroxybutyrate) in Escherichia coli. Biotechnol Prog 22: 420-425.
65. Sauer, U., Lasko, D.R., Fiaux, J., Hochuli, M., Glaser, R., Szyperski, T., etal. (1999) Metabolic flux ratio analysis of genetic and environmental modulations of Escherichia coli central carbon metabolism. J Bacteriol 181: 6679-6688.
66. Schlegel, H.G., and Gottschalk, G. (1962) Poly-β-hydroxybuttersäure, ihre Verbreitung, Funktion und Biosynthese. Angew Chem 74: 342-347.
67. Schubert, P., Steinbüchel, A., and Schlegel, H.G. (1988) Cloning of the Alcaligenes eutrophus genes for synthesis of poly-b-hydroxybutyric acid (PHB) and synthesis of PHB in Escherichia coli. J Bacteriol 170: 5837-5847.
68. Searle, P.L. (1984) The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. A review. Analyst 109: 549-568.
69. Senior, P.J., and Dawes, E.A. (1973) The regulation of poly-b-hydroxybutyrate metabolism in Azotobacter beijerinckii. Biochem J 134: 225-238.
70. Serafim, L.S., Lemos, P.C., Albuquerque, M.G.E., and Reis, M.A.M. (2008) Strategies for PHA production by mixed cultures and renewable waste materials. Appl Microbiol Biotechnol 81: 615-628.
71. Shah, A.A., Hasan, F., Hameed, A., and Ahmed, S. (2008) Biological degradation of plastics: a comprehensive review. Biotechnol Adv 26: 246-265.
72. Shen, L.C., and Atkinson, D.E. (1970) Regulation of pyruvate dehydrogenase from Escherichia coli. Interactions of adenylate energy charge and other regulatory parameters. J Biol Chem 245: 5974-5978.
73. Sivan, A. (2011) New perspectives in plastic biodegradation. Curr Opin Biotechnol 22: 422-426.
74. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
75. Smyth, G.K., and Speed, T. (2003) Normalization of cDNA microarray data. Methods 31: 265-273.
76. Sohn, S.B., Kim, T.Y., Park, J.M., and Lee, S.Y. (2010) In silico genome-scale metabolic analysis of Pseudomonas putida KT2440 for polyhydroxyalkanoate synthesis, degradation of aromatics and anaerobic survival. Biotechnol J 5: 739-750.
77. Suriyamongkol, P., Weselake, R., Narine, S., Moloney, M., and Shah, S. (2007) Biotechnological approaches for the production of polyhydroxyalkanoates in microorganisms and plants - a review. Biotechnol Adv 25: 148-175.
78. Walshaw, D.L., Wilkinson, A., Mundy, M., Smith, M., and Poole, P.S. (1997) Regulation of the TCA cycle and the general amino acid permease by overflow metabolism in Rhizobium leguminosarum. Microbiology 143: 2209-2221.
79. Witholt, B., and Kessler, B. (1999) Perspectives of medium chain length poly(hydroxyalkanoates), a versatile set of bacterial bioplastics. Curr Opin Biotechnol 10: 279-285.
80. Wolfe, A.J. (2005) The acetate switch. Microbiol Mol Biol Rev 69: 12-12.
81. Wu, X., Monchy, S., Taghavi, S., Zhu, W., Ramos, J., and van der Lelie, D. (2011) Comparative genomics and functional analysis of niche-specific adaptation in Pseudomonas putida. FEMS Microbiol Rev 35: 299-323.
82. Yang, Y.H., Dudoit, S., Luu, P., Lin, D.M., Peng, V., Ngai, J., and Speed, T.P. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15.
83. Yu, J., and Si, Y. (2004) Metabolic carbon fluxes and biosynthesis of polyhydroxyalkanoates in Ralstonia eutropha on short chain fatty acids. Biotechnol Prog 20: 1015-1024.
84. Yuste, L., Hervás, A.B., Canosa, I., Tobes, R., Jiménez, J.I., Nogales, J., etal. (2006) Growth phase-dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analysed with a genome-wide DNA microarray. Environ Microbiol 8: 165-177.
85. Zamboni, N., Fischer, E., and Sauer, U. (2005) FiatFlux - a software for metabolic flux analysis from 13C-glucose experiments. BMC Bioinformatics 6: 209.