Versatile metabolic adaptations of Ralstonia eutropha H16 to a loss of PdhL, the E3 component of the pyruvate dehydrogenase complex

Applied and Environmental Microbiology

Volumn 77, Issue 7, 2011, Pages 2254-2263

  Raberg, Matthias ^a   Bechmann, Jan ^a   Brandt, Ulrike ^a   Schlüter, Jonas ^a   Uischner, Bianca ^a   Voigt, Birgit ^b   Hecker, Michael ^b   Steinbüchel, Alexander ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3-HYDROXYBUTYRIC ACID; BURKHOLDERIA CEPACIA; CELLULAR LEVELS; CODING GENES; COMPLEMENTATION; DELETION MUTANTS; DIMERIZATION DOMAIN; GENOME ANALYSIS; GENOME SEQUENCES; GROWTH BEHAVIOR; IN-SILICO; INACTIVE ENZYMES; METABOLIC ADAPTATION; MULTIENZYME COMPLEXES; MUTANT PHENOTYPE; POLAR EFFECT; PROTEOMES; PYRUVATE DEHYDROGENASE COMPLEX; RALSTONIA EUTROPHA; SYNTHESIS RATE; WILD TYPES;

BACTERIA; ENZYMES;

GENE ENCODING;

PROTEIN SUBUNIT; PROTEOME; PYRUVATE DEHYDROGENASE COMPLEX;

ADAPTATION; BACTERIUM; ENZYME ACTIVITY; GENOME; METABOLISM; PHENOTYPE; PLASMID;

ARTICLE; BURKHOLDERIA CEPACIA; CUPRIAVIDUS NECATOR; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLASMID; TRANSPOSON;

BURKHOLDERIA CEPACIA; CUPRIAVIDUS NECATOR; DNA TRANSPOSABLE ELEMENTS; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; MUTAGENESIS, INSERTIONAL; PLASMIDS; PROTEIN SUBUNITS; PROTEOME; PYRUVATE DEHYDROGENASE COMPLEX;

BURKHOLDERIA CEPACIA; CUPRIAVIDUS NECATOR;

EID: 79953268441     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02360-10     Document Type: Article

References (71)

1. Abe, T., T. Kobayashi, and T. Saito. 2005. Properties of a novel intracellular poly(3-hydroxybutyrate) depolymerase with high specific activity (PhaZd) in Wautersia eutropha H16. J. Bacteriol. 187:6982-6990.
2. Aevarsson, A., K. Seger, S. Turley, J. R. Sokatch, and W. G. Hol. 1999. Crystal structure of 2-oxoisovalerate and dehydrogenase and the architecture of 2-oxo acid dehydrogenase multienzyme complexes. Nat. Struct. Biol. 6:785-792.
3. Anderson, A. J., and E. A. Dawes. 1990. Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol. Rev. 54:450-472.
4. Aragno, M., A. Walther-Mauruschat, F. Mayer, and H. G. Schlegel. 1977. Micromorphology of Gram-negative hydrogen bacteria. I. Cell morphology and flagellation. Arch. Microbiol. 114:93-100.
5. Berg, A., and A. de Kok. 1997. 2-Oxoacid dehydrogenase multienzyme complexes. The central role of the lipoyl domain. Biol. Chem. 378:617-634.
6. Bergmeyer, H. U. 1974. Methoden der enzymatischen Analyse. Verlag Chemie, Weinheim, Germany.
7. Berth, M., F. M. Moser, M. Kolbe, and J. Bernhardt. 2007. The state of the art in the analysis of two-dimensional gel electrophoresis images. Appl. Microbiol. Biotechnol. 76:1223-1243.
8. 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.
9. Brandl, H., R. A. Gross, R. W. Lenz, and R. C. Fuller. 1988. Pseudomonas oleovorans as a source of poly(β-hydroxyalkanoates) for potential applications as biodegradable polyesters. Appl. Environ. Microbiol. 54:1977-1982.
10. Budde, C. F., A. E. Mahan, J. Lu, C. Rha, and A. J. Sinskey. 2010. Roles of multiple acetoacetyl coenzyme A reductases in polyhydroxybutyrate biosynthesis in Ralstonia eutropha H16. J. Bacteriol. 192:5319-5328.
11. Carothers, D. J., G. Pons, and M. S. Patel. 1989. Dihydrolipoamide dehydrogenase: functional similarities and divergent evolution of the pyridine nucleotide-disulfide oxidoreductases. Arch. Biochem. Biophys. 268:409-425.
12. Cramm, R. 2009. Genomic view of energy metabolism in Ralstonia eutropha H16. J. Mol. Microbiol. Biotechnol. 16:38-52.
13. Czok, R., and W. Lamprecht. 1974. Pyruvate, phosphoenolpyruvate, and D-glycerate-2-phosphate, p. 1446-1451. In H. U. Bergmeyer (ed.), Methods of enzymatic analysis, 2nd ed., vol. 3. Academic Press, New York, NY.
14. de Kok, A., A. F. Hengeveld, A. Martin, and A. H. Westphal. 1998. The pyruvate dehydrogenase multi-enzyme complex from Gram-negative bacteria. Biochim. Biophys. Acta 1385:353-366.
15. Doi, Y., A. Segawa, S. Nakamura, and M. T. Kunioka. 1990. Production of biodegradable copolyesters by Alcaligenes eutrophus, p. 37-48. In E. A. Dawes (ed.), New biosynthetic biodegradable polymers of industrial interest from microorganisms. Kluyver, Dordrecht, Netherlands.
16. Douce, R., J. Bourguignon, M. Neuburger, and F. Rebeille. 2001. The glycine decarboxylase system: a fascinating complex. Trends. Plant Sci. 6:167-176.
17. Fründ, C., H. Priefert, A. Steinbüchel, and H. G. Schlegel. 1989. Biochemical and genetic analyses of acetoin catabolism in Alcaligenes eutrophus. J. Bacteriol. 171:6539-6548.
18. Haywood, G. W., A. J. Anderson, L. Chu, and A. E. Dawes. 1988. Characterization of two 3-ketothiolases possessing differing substrate specificities in the polyhydroxyalcanoate synthesizing organism Alcaligenes eutrophus. FEMS Microbiol. Lett. 52:91-96.
19. Haywood, G. W., A. J. Anderson, L. Chu, and A. E. Dawes. 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.
20. Haywood, G. W., A. J. Anderson, and A. E. Dawes. 1989. The importance of PHB synthase substrate specificity in polyhydroxyalkanoate synthesis by Alcaligenes eutrophus. FEMS Microbiol. Lett. 57:1-6.
21. Hein, S., and A. Steinbüchel. 1994. Biochemical and molecular characterization of the Alcaligenes eutrophus pyruvate dehydrogenase complex and identification of a new type of dihydrolipoamide dehydrogenase. J. Bacteriol. 176:4394-4408.
22. Hein, S., and A. Steinbüchel. 1996. Alcaligenes eutrophus possesses a second pyruvate dehydrogenase (E1). Eur. J. Biochem. 237:674-684.
23. Hocking, P. J., and R. H. Marchessault. 1994. Biopolyesters, p. 48-96. In G. J. L. Griffin (ed.), Chemistry and technology of biodegradable polymers. Chapman & Hall, London, United Kingdom.
24. Holzer, H. 1961. Wirkungsmechanismus von Thiaminpyrophosphat. Angew. Chem. 73:721-727.
25. Knapp, J. E., et al. 2000. Expression, purification, and structural analysis of the trimeric form of the catalytic domain of the Escherichia coli dihydrolipoamide succinyltransferase. Protein Sci. 9:37-48.
26. Kobayashi, T., K. Uchino, T. Abe, Y. Yamazaky, and T. Saito. 2005. Novel intracellular 3-hydroxybutyrate-oligomer hydrolase in Wautersia eutropha H16. J. Bacteriol. 187:5129-5135.
27. Kovach, M. E., et al. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
28. Kunioka, M., Y. Nakamura, and Y. Doi. 1988. New bacterial copolyesters produced in Alcaligenes eutrophus from organic acids. Polym. Commun. 29:174-176.
29. Lee, S. Y., and S. J. Park. 2005. Fermentative production of short-chainlength PHAs, p. 207-234. In A. Steinbüchel and Y. Doi (ed.), Biotechnology of biopolymers-from synthesis to patents, vol. 1. Wiley-VCH, Weinheim, Germany.
30. Li, M., P. Y. Ho, S. Yao, and K. Shimizu. 2006. Effect of lpdA gene knockout on the metabolism in Escherichia coli based on enzyme activities, intracellular metabolite concentrations and metabolic flux analysis by 13C-labeling experiments. J. Biotechnol. 122:254-266.
31. Lindsay, H., et al. 2000. FAD insertion is essential for attaining the assembly competence of the dihydrolipoamide dehydrogenase (E3) monomer from Escherichia coli. J. Biol. Chem. 275:36665-36670.
32. MacFarlane, S. A., and M. Merrick. 1985. The nucleotide sequence of the nitrogen regulation gene ntrB and the glnA-ntrBC intergenic region of Klebsiella pneumoniae. Nucleic Acids Res. 13:7591-7606.
33. Madison, L. L., and G. W. Huisman. 1999. Metabolic engineering of poly(3- hydroxyalkanoates): from DNA to plastic. Microbiol. Mol. Biol. Rev. 63:21-53.
34. Mattevi, A., G. Obmolova, J. R. Sokatch, C. Betzel, and W. G. Hol. 1992. The refined crystal structure of Pseudomonas putida lipoamide dehydrogenase complexed with NAD+t 2.45 Å resolution. Proteins 13:336-351.
35. Mattevi, A., A. J. Schierbeek, and W. G. Hol. 1991. Refined crystal structure of lipoamide dehydrogenase from Azotobacter vinelandii at 2-2 A resolution. J. Mol. Biol. 220:975-994.
36. Misra, T. K., et al. 1985. Mercuric reductase structural genes from plasmid R100 and transposon Tn501: functional domains of the enzyme. Gene 34: 253-262.
37. Nakai, T., S. Kuramitsu, and N. Kamiya. 2008. Structural bases for the specific interactions between the E2 and E3 components of the Thermus thermophilus 2-oxo acid dehydrogenase complexes. J. Biochem. 143:747-758.
38. Oeding, V., and H. G. Schlegel. 1973. β-Ketothiolase from Hydrogenomonas eutrophus H16 and its significance in the regulation of poly-β-hydroxybutyrate metabolism. Biochem. J. 134:239-248.
39. Oppermann, F. B., B. Schmidt, and A. Steinbüchel. 1991. Purification and characterization of acetoin:2,6-dichlorophenolindophenol oxidoreductase, dihydrolipoamide dehydrogenase, and dihydrolipoamide acetyltransferase of the Pelobacter carbinolicus acetoin dehydrogenase enzyme system. J. Bacteriol. 173:757-767.
40. Patel, M. S., and L. G. Korotchkina. 2003. The biochemistry of the pyruvate dehydrogenase complex. Biochem. Mol. Biol. Educ. 31:5-15.
41. Peoples, O. P., and A. J. Sinskey. 1989. Poly-β-hydroxybutyrate biosynthesis in Alcaligenes eutrophus H16. Characterization of the genes encoding β-ketothiolase and acetoacetyl-CoA reductase. J. Biol. Chem. 263:15293-15297.
42. Peoples, O. P., and A. J. Sinskey. 1989. Poly-β-hydroxybutyrate biosynthesis in Alcaligenes eutrophus H16. Identification and characterization of the PHB polymerase gene (phbC). J. Biol. Chem. 264:15298-15303.
43. Pohlmann, A., et al. 2006. Hydrogen-based biotechnology: genome sequence of the bioplastic-producing "Knallgas" bacterium Ralstonia eutropha H16. Nat. Biotechnol. 24:1257-1262.
44. Pötter, M., H. Müller, and A. Steinbüchel. 2005. Influence of homologous phasins (PhaP) on PHA accumulation and regulation of their expression by the transcriptional repressor PhaR in Ralstonia eutropha H16. Microbiology 151:825-833.
45. Pratt, C. W., D. Voet, and J. G. Voet. 2005. Fundamentals of biochemistry: life at the molecular level. John Wiley & Sons, New York, NY.
46. Pries, A., S. Hein, and A. Steinbüchel. 1992. Identification of a lipoamide dehydrogenase gene as second locus affected in poly(3-hydroxybutyric acid)-leaky mutants of Alcaligenes eutrophus. FEMS Microbiol. Lett. 76:227-233.
47. Raberg, M., et al. 2008. Ralstonia eutropha H16 flagellation changes according to nutrient supply and state of poly(3-hydroxybutyrate) accumulation. Appl. Environ. Microbiol. 74:4477-4490.
48. Rabilloud, T. 1999. Proteome research: two-dimensional gel electrophoresis and identification methods (principles and practice). Springer, Berlin, Germany.
49. Rajashankar, K. R., et al. 2005. Crystal structure and functional analysis of lipoamide dehydrogenase from Mycobacterium tuberculosis. J. Biol. Chem. 280:33977-33983.
50. Reese, M. G. 2001. Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput. Chem. 26:51-56.
51. Reinecke, F., and A. Steinbüchel. 2009. Ralstonia eutropha H16 strain H16 as model organism for PHA metabolism and for biotechnological production of technically interesting biopolymers. J. Mol. Microbiol. Biotechnol. 16:91-108.
52. Ricaud, P. M., M. J. Howard, E. L. Roberts, R. W. Broadhurst, and R. N. Perham. 1996. Three-dimensional structure of the lipoyl domain from the dihydrolipoyl succinyltransferase component of the 2-oxoglutarate dehydrogenase multienzyme complex of Escherichia coli. J. Mol. Biol. 264:179-190.
53. Rice, D. W., G. E. Schulz, and J. R. Guest. 1984. Structural relationship between glutathione reductase and lipoamide dehydrogenase. J. Mol. Biol. 174:483-496.
54. Saegusa, H., M. Shiraki, C. Kanai, and T. Saito. 2001. Cloning of an intracellular poly[D-(-)-3-hydroxybutyrate] depolymerase gene from Ralstonia eutropha H16 and characterization of the gene product. J. Bacteriol. 183:94-100.
55. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Schlegel, H. G., H. Kaltwasser, and G. Gottschalk. 1961. Ein Submersverfahren zur Kultur wasserstoffoxidierender Bakterien: Wachstumsphysiologische Untersuchungen. Arch. Mikrobiol. 38:209-222.
57. Schlegel, H. G., R. Lafferty, and I. Krauss. 1970. The isolation of mutants not accumulating poly-β-hydroxybutyric acid. Arch. Mikrobiol. 71:283-294.
58. Schreiner, M. E., D. Fiur, J. Holatko, M. Patek, and B. J. Eikmanns. 2005. E1 enzyme of the pyruvate dehydrogenase complex in Corynebacterium glutamicum: molecular analysis of the gene and phylogenetic aspects. J. Bacteriol. 187:6005-6018.
59. Schubert, P., A. Steinbüchel, and H. G. Schlegel. 1988. Cloning of the Alcaligenes eutrophus genes for synthesis of poly-β-hydroxybutyric acid (PHB) and synthesis of PHB in Escherichia coli. J. Bacteriol. 170:5837-5847.
60. Shevchenko, A., O. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
61. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic-engineering-transposon mutagenesis in gramnegative bacteria. Biotechnology 1:784-791.
62. Slater, T., et al. 1998. Multiple β-ketothiolases mediate poly(β-hydroxyalkanoate) copolymer synthesis in Ralstonia eutropha. J. Bacteriol. 180:1979-1987.
63. Steinbüchel, A., and B. Füchtenbusch. 1998. Bacterial and other biological systems for polyester production. Trends Biotechnol. 16:419-427.
64. Steinbüchel, A., and H. G. Schlegel. 1989. Excretion of pyruvate by mutants of Alcaligenes eutrophus, which are impaired in the accumulaton of poly(β-hydroxybutyric acid) (PHB), under conditions permitting synthesis of PHB. Appl. Microbiol. Biotechnol. 31:168-175.
65. Steinbüchel, A., and H. E. Valentin. 1995. Diversity of microbial polyhydroxyalkanoic acids. FEMS Microbiol. Lett. 128:219-228.
66. Timm, A., and A. Steinbüchel. 1990. Formation of polyesters consisting of medium-chain-length 3-hydroxyalkanoic acids from gluconate by Pseudomonas aeruginosa and other fluorescent pseudomonads. Appl. Environ. Microbiol. 56:3360-3367.
67. Uchino, K., T. Saito, B. Gebauer, and D. Jendrossek. 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.
68. Voigt, B., et al. 2006. The extracellular proteome of Bacillus licheniformis grown in different media and under different nutrient starvation conditions. Proteomics 6:268-281.
69. von Heijne, G. 1989. The structure of signal peptides from bacterial lipoproteins. Protein Eng. 2:531-534.
70. Williams, S. F., and D. P. Martin. 2002. Applications of PHAs in medicine and pharmacy, p. 91-127. In Y. Doi and A. Steinbüchel (ed.), Biopolymers, vol. 4. Polyesters III-applications and commercial products. Wiley-VCH, Weinheim, Germany.
71. York, G. M., et al. 2003. Ralstonia eutropha H16 encodes two and possibly three intracellular poly[D-(-)-3-hydroxybuturate] depolymerase genes. J. Bacteriol. 185:3788-3794.