Tight coupling of polymerization and depolymerization of polyhydroxyalkanoates ensures efficient management of carbon resources in Pseudomonas putida

Microbial Biotechnology

Volumn 6, Issue 5, 2013, Pages 551-563

  Arias, Sagrario ^a   Bassas Galia, Monica ^a   Molinari, Gabriella ^a   Timmis, Kenneth N ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; POLYHYDROXYALKANOIC ACID;

ARTICLE; DEPOLYMERIZATION; GENE ACTIVITY; GENE EXPRESSION; NONHUMAN; OPERON; POLYMERIZATION; PSEUDOMONAS PUTIDA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRUCTURAL GENE; SYNTHESIS;

EID: 84882285580     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12040     Document Type: Article

References (55)

1. Arias, S., and Bassas, M. (2010) Rediscovering biopolymers. In Handbook of Hydrocarbon and Lipid Microbiology: Consequences of Microbial Interactions with Hydrocarbons Oils, Fats and Lipids. Timmis, K.N. (ed.). Berlin, Germany: Springer Verlag, pp. 2967-2980.
2. Arias, S., Sandoval, A., Arcos, M., Cañedo, M.L., Naharro, G., and Luengo, J.M. (2008) Poly-3-hydroxyalkanoate synthases from Pseudomonas putida U: substrate specificity and ultrastructural studies. Microb Biotechnol 1: 170-176.
3. Bassas, M. (2010) Isolation and analysis of storage compounds. In Handbook of Hydrocarbon and Lipid Microbiology: Experimental Protocols and Appendices. Timmis, K.N. (ed.). Berlin, Germany: Springer Verlag, pp. 3725-3741.
4. Bassas-Galia, M., Nogales, B., Arias, S., Rohde, M., Timmis, K.T., and Molinari, G. (2012) Plant original Massilia isolates producing polyhydroxybutyrate, including one exhibiting high yields from glycerol. J Appl Microbiol 112: 443-454.
5. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., etal. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
6. Cai, L., Yuan, M.Q., Liu, F., Jian, J., and Chen, G.Q. (2009) Enhanced production of medium-chain-length polyhydroxyalkanoates (PHA) by PHA depolymerase knockout mutant of Pseudomonas putida KT2442. Bioresour Technol 100: 2265-2270.
7. Cheema, S., Bassas-Galia, M., Sarma, P.M., Lal, B., and Arias, S. (2012) Exploiting metagenomic diversity for novel polyhydroxyalkanoate synthases: production of a terpolymer poly(3-hydroxybutyrate-co-3-hydroxyhexanoate-co-3-hydroxyoctanoate) with a recombinant Pseudomonas putida strain. Bioresour Technol 103: 322-328.
8. Ciesielski, S., Pokoj, T., and Klimiuk, E. (2010) Cultivation-dependent and -independent characterization of microbial community producing polyhydroxyalkanoates from raw-glycerol. J Microbiol Biotechnol 20: 853-861.
9. Conte, E., Catara, V., Greco, S., Russo, M., Alicata, R., Strano, L., etal. (2006) Regulation of polyhydroxyalkanoate synthases (phaC1 and phaC2) gene expression in Pseudomonas corrugata. Appl Microbiol Biotechnol 72: 1054-1062.
10. Diederich, L., Roth, A., and Messer, W. (1994) A versatile plasmid vector system for the regulated expression of genes in Escherichia coli. Biotechniques 16: 916-923.
11. Donnenberg, M.S., and Kaper, J.B. (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59: 4310-4317.
12. de Eugenio, L.I., Escapa, I.F., Morales, V., Dinjaski, N., Galán, B., García, J.L., and Prieto, M.A. (2010a) 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.
13. de Eugenio, L.I., Galán, B., Escapa, I.F., Maestro, B., Sanz, J.M., García, J.L., and Prieto, M.A. (2010b) The PhaD regulator control the simultaneous expression of the pha genes involved in polyhydroxyalkanoates metabolism and turnover in Pseudomonas putida KT2442. Environ Microbiol 12: 1591-1603.
14. 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.
15. García, B., Olivera, E.R., Minambres, B., Fernández-Valverde, M., Cañedo, L.M., Prieto, M.A., etal. (1999) Novel biodegradable aromatic plastics from a bacterial source. Genetic and biochemical studies on a route of the phenylacetyl-CoA catabolon. J Biol Chem 274: 29228-29241.
16. Grage, K., Jahns, A.C., Parlane, N., Palanisamy, R., Rasiah, I.A., Atwood, J.A., and Rehm, B.H. (2009) Bacterial polyhydroxyalkanoate granules: biogenesis, structure, and potential use as nano-/micro-beads in biotechnological and biomedical applications. Biomacromolecules 10: 660-669.
17. Harayama, S., Rekik, M., Wubbolts, M., Rose, K.R., Leppik, R.A., and Timmis, K.N. (1989) Characterization of five genes in the upper-pathway operon of TOL plasmid pWW0 from Pseudomonas putida and identification of the gene products. J Bacteriol 171: 5048-5055.
18. Haywood, G.W., Anderson, A.J., Ewing, D.F., and Dawes, E.A. (1990) Accumulation of a polyhydroxyalkanoate containing primarily 3-hydroxydecanoate from simple carbohydrate substrates by Pseudomonas sp. strain NCIMB 40135. Appl Environ Microbiol 56: 3354-3359.
19. Herrero, M., de Lorenzo, V., and Timmis, K.N. (1990) Transposon vector containing non-antibiotic selection markers for cloning and stable chromosomal insertion of foreign DNA in gram-negative bacteria. J Bacteriol 172: 6557- 6567.
20. Herrero, M., de Lorenzo, V., Ensley, B., and Timmis, K.N. (1993) A T7 RNA polymerase-based system for the construction of Pseudomonas strains with phenotypes dependent on TOL-meta pathway effecters. Gene 134: 103-106.
21. Hoffmann, N., and Rehm, B.H. (2005) Nitrogen-dependent regulation of medium-chain length polyhydroxyalkanoate biosynthesis genes in Pseudomonads. Biotechnol Lett 27: 279-282.
22. Huisman, G.W., Wonink, E., Meima, R., Kazemier, B., Terpstra, P., and Witholt, B. (1991) Metabolism of poly(3-hydroxyalkanoates) by Pseudomonas oleovorans. Identification and sequences of genes and function of the encoded proteins in the synthesis and degradation of PHA. J Biol Chem 266: 2191-2198.
23. Hume, A.R., Nikodinovic-Runic, J., and O'Connor, K.E. (2009) FadD from Pseudomonas putida CA-3 is a true long-chain fatty acyl coenzyme A synthetase that activates phenylalkanoic and alkanoic acids. J Bacteriol 191: 7554-7565.
24. Kim, D.Y., Kim, H.W., Chung, M.G., and Rhee, Y.H. (2007) Biosynthesis, modification, and biodegradation of bacterial medium-chain-length polyhydroxyalkanoates. J Microbiol 45: 87-97.
25. Kim, T.K., Jung, Y.M., Vo, M.T., Shioya, S., and Lee, Y.H. (2006) Metabolic engineering and characterization of phaC1 and phaC2 genes from Pseudomonas putida KCTC1639 for overproduction of medium-chain-length polyhydroxyalkanoate. Biotechnol Prog 22: 1541-1546.
26. Klinke, S., de Roo, G., Witholt, B., and Kessler, B. (2000) Role of phaD in accumulation of medium-chain-length poly(3-hydroxyalkanoates) in Pseudomonas oleovorans. Appl Environ Microbiol 66: 3705-3710.
27. Kraak, M.N., Kessler, B., and Witholt, B. (1997) In vitro activities of granule bound poly-(R)-3-hydroxyalkanoate) polymerase C1 of Pseudomonas oleovorans. Development of an activity test for medium-chain-length-Poly(3-hydroxyalkanoate) polymerases. Eur J Biochem 250: 432-439.
28. Luengo, J.M., García, B., Sandoval, A., Naharro, G., and Olivera, E.R. (2003) Bioplastics from microorganisms. Curr Opin Microbiol 6: 251-260.
29. 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.
30. Martínez-Blanco, H., Reglero, A., Rodríguez-Aparicio, L.B., and Luengo, J.M. (1990) Purification and biochemical characterization of phenylacetyl-CoA ligase from Pseudomonas putida. A specific enzyme for the catabolism of phenylacetic acid. J Biol Chem 265: 7084-7090.
31. Neumann, L., Spinozzi, F., Sinibaldi, R., Rustichelli, F., Pötter, M., and Steinbüchel, A. (2008) Binding of the major phasin, PhaP1, from Ralstonia eutropha H16 to poly(3-hydroxybutyrate) granules. J Bacteriol 190: 2911-2919.
32. Olivera, E.R., Carnicero, D., García, B., Miñambres, B., Moreno, M.A., Cañedo, L., etal. (2001a) Two different pathways are involved in the beta-oxidation of n-alkanoic and n-phenylalkanoic acids in Pseudomonas putida U: genetic studies and biotechnological applications. Mol Microbiol 39: 863-874.
33. Olivera, E.R., Carnicero, D., Jodra, R., Miñambres, B., García, B., Abraham, G.A., etal. (2001b) Genetically engineered Pseudomonas: a factory of new bioplastics with broad applications. Environ Microbiol 3: 612-618.
34. Pieper-Fürst, U., Madkour, M.H., Mayer, F., and Steinbüchel, A. (1995) Identification of the region of a 14-kilodalton protein of Rhodococcus ruber that is responsible for the binding of this phasin to polyhydroxyalkanoic acid granules. J Bacteriol 177: 2513-2523.
35. Pötter, M., and Steinbüchel, A. (2005) Poly(3-hydroxybutyrate) granule-associated proteins: impacts on poly(3-hydroxybutyrate) synthesis and degradation. Biomacromolecules 6: 552-560.
36. Prieto, M.A., Bühler, B., Jung, K., Witholt, B., and Kessler, B. (1999a) PhaF, a polyhydroxyalkanoate-granule-associated protein of Pseudomonas oleovorans GPo1 involved in the regulatory expression system for pha genes. J Bacteriol 181: 858-868.
37. Prieto, M.A., Kellerhals, M.B., Bozzato, G.B., Radnovic, D., Witholt, B., and Kessler, B. (1999b) Engineering of stable recombinant bacteria for production of chiral medium-chain-length poly-3-hydroxyalkanoates. Appl Environ Microbiol 65: 3265-3271.
38. Quant, J., and Hynes, M.F. (1983) Versatile suicide vectors which allow direct selection for gene replacement in Gram negative bacteria. Gene 127: 15-21.
39. Reis, M.A., Serafim, L.S., Lemos, P.C., Ramos, A.M., Aguair, F.R., and Van Loosdrecht, M.C. (2003) Production of polyhydroxyalkanoates by mixed microbial cultures. Bioprocess Biosyst Eng 25: 377-385.
40. Ren, Q., de Roo, G., Ruth, K., Witholt, B., Zinn, M., and Thöny-Meyer, L. (2009a) Simultaneous accumulation and degradation of polyhydroxyalkanoates: futile cycle or clever regulation? Biomacromolecules 10: 916-922.
41. Ren, Q., de Roo, G., Witholt, B., Zinn, M., and Thöny-Meyer, L. (2009b) Overexpression and characterization of medium-chain-length polyhydroxyalkanoate granule bound polymerases from Pseudomonas putida GPo1. Microb Cell Fact 19: 8-60.
42. Ren, Q., de Roo, G., Witholt, B., Zinn, M., and Thöny-meyer, L. (2010) Influence of growth stage on activities of polyhydroxyalkanoate (PHA) polymerase and PHA depolymerase in Pseudomonas putida U. BMC Microbiol 10: 254.
43. 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.
44. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, NY, USA: CSHL Press.
45. Sánchez-Romero, J.M., Díaz-Orejas, R., and de Lorenzo, V. (1998) Resistance to tellurite as a selection marker for genetic manipulations of Pseudomonas strains. Appl Environ Microbiol 64: 4040-4046.
46. Sandoval, A., Arias-Barrau, E., Bermejo, F., Cañedo, L., Naharro, G., Olivera, E.R., and Luengo, J.M. (2005) Production of 3-hydroxy-n-phenylalkanoic acids by a genetically engineered strain of Pseudomonas putida. Appl Microbiol Biotechnol 67: 97-105.
47. Sandoval, A., Arias-Barrau, E., Arcos, M., Naharro, G., Olivera, E.R., and Luengo, J.M. (2007) Genetic and ultrastructural analysis of different mutants of Pseudomonas putida affected in the poly-3-hydroxy-n-alkanoate gene cluster. Environ Microbiol 9: 737-751.
48. Selvaraj, J., and Iyer, V.N. (1983) Suicide plasmid vehicles for insertion mutagenesis in Rhizobium mellioti and related bacteria. J Bacteriol 156: 1292-1300.
49. Solaiman, D.K., Ashby, R.D., and Foglia, T.A. (2003) Effect of inactivation of poly(hydroxyalkanoates) depolymerase gene on the properties of poly(hydroxyalkanoates) in Pseudomonas resinovorans. Appl Microbiol Biotechnol 62: 536-543.
50. Steinbüchel, A., Aerts, K., Babel, W., Follner, C., Liebergesell, M., Madkour, M.H., etal. (1995) Considerations on the structure and biochemistry of bacterial polyhydroxyalkanoic acid inclusions. Can J Microbiol 41: 94-105.
51. Timm, A., and Steinbüchel, A. (1992) Cloning and molecular analysis of the poly(3-hydroxyalkanoic acid) gene locus of Pseudomonas aeruginosa PAO1. Eur J Biochem 209: 15-30.
52. Uchino, K., Saito, T., Gebauer, B., and Jendrossek, D. (2007) Isolated poly(3-hydroxybutyrate) (PHB) granules are complex bacterial organelles catalyzing formation of PHB from acetyl coenzyme A (CoA) and degradation of PHB to acetyl-CoA. J Bacteriol 189: 8250-8256.
53. Velázquez, F., Pflüger, K., Cases, I., de Eugenio, L.I., and de Lorenzo, V. (2007) The phosphotransferase system formed by PtsP, PtsO, and PtsN proteins controls production of polyhydroxyalkanoates in Pseudomonas putida. J Bacteriol 189: 4529-4533.
54. Wieczorek, R., Pries, A., Steinbüchel, A., and Mayer, F. (1995) Analysis of a 24-kilodalton protein associated with the polyhydroxyalkanoic acid granules in Alcaligenes eutrophus. J Bacteriol 177: 2425-2435.
55. York, G.M., Stubbe, J., and Sinskey, A.J. (2002) The Ralstonia eutropha PhaR protein couples synthesis of the PhaP phasin to the presence of polyhydroxybutyrate in cells and promotes polyhydroxybutyrate production. J Bacteriol 184: 59-66.