Regulation of the malic enzyme gene malE by the transcriptional regulator MalR in Corynebacterium glutamicum

Journal of Biotechnology

Volumn 159, Issue 3, 2012, Pages 204-215

  Krause, Jens P ^a   Polen, Tino ^b   Youn, Jung Won ^a,d   Emer, Denise ^c   Eikmanns, Bernhard J ^c   Wendisch, Volker F ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c UNIVERSITY OF ULM   (Germany)

^d UNIVERSITY OF STUTTGART   (Germany)

Author keywords

Corynebacterium glutamicum; MalE; Malic enzyme; MalR; Transcriptional regulation

Indexed keywords

CORYNEBACTERIUM GLUTAMICUM; MALE; MALIC ENZYMES; MALR; TRANSCRIPTIONAL REGULATION;

AMINO ACIDS; CARBOXYLATION; DNA; EXPERIMENTS; GENE ENCODING; GLUCOSE; PURIFICATION;

ENZYMES;

FUMARIC ACID; GLUCOSE; MALATE DEHYDROGENASE (DECARBOXYLATING); MALIC ACID; PYRUVIC ACID; SUCCINIC ACID;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; CORYNEBACTERIUM GLUTAMICUM; DNA BINDING; GENE DELETION; GENE EXPRESSION REGULATION; MUTATIONAL ANALYSIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; BASE SEQUENCE; CONSENSUS SEQUENCE; CORYNEBACTERIUM GLUTAMICUM; MALATE DEHYDROGENASE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; SEQUENCE DELETION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); CORYNEBACTERIUM GLUTAMICUM; POSIBACTERIA;

EID: 84860839960     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2012.01.003     Document Type: Article

References (67)

1. Ajinomoto, 2010. Feed-Use Amino Acids Business. (cited 13.10.11). http://www.ajinomoto.com/ir/pdf/Feed-useAA-Oct2010.pdf.
2. Ajinomoto, 2010. Food Products Business. (cited 13.10.11). http://www.ajinomoto.com/ir/pdf/Food-Oct2010.pdf.
3. Alekshun M.N., Levy S.B. Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. J. Bacteriol. 1999, 181:4669-4672.
4. Auchter M., Cramer A., Hüser A., Rückert C., Emer D., Schwarz P., Arndt A., Lange C., Kalinowski J., Wendisch V.F., Eikmanns B.J. RamA and RamB are global transcriptional regulators in Corynebacterium glutamicum and control genes for enzymes of the central metabolism. J. Biotechnol. 2011, 154:126-139.
5. Bailey T.L., Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1994, 2:28-36.
6. Becker J., Klopprogge C., Wittmann C. Metabolic responses to pyruvate kinase deletion in lysine producing Corynebacterium glutamicum. Microb. Cell Fact. 2008, 7:8.
7. Blombach B., Riester T., Wieschalka S., Ziert C., Youn J.-W., Wendisch V.F., Eikmanns B.J. Corynebacterium glutamicum tailored for efficient isobutanol production. Appl. Environ. Microbiol. 2011, 77:3300-3310.
8. Bologna F.P., Andreo C.S., Drincovich M.F. Escherichia coli malic enzymes: two isoforms with substantial differences in kinetic properties, metabolic regulation, and structure. J. Bacteriol. 2007, 189:5937-5946.
9. Brinkrolf K., Brune I., Tauch A. The transcriptional regulatory network of the amino acid producer Corynebacterium glutamicum. J. Biotechnol. 2007, 129:191-211.
10. Brinkrolf K., Plöger S., Solle S., Brune I., Nentwich S.S., Hüser A.T., Kalinowski J., Pühler A., Tauch A. The LacI/GalR family transcriptional regulator UriR negatively controls uridine utilization of Corynebacterium glutamicum by binding to catabolite-responsive element (cre)-like sequences. Microbiology 2008, 154:1068-1081.
11. Buchinger S., Strösser J., Rehm N., Hänssler E., Hans S., Bathe B., Schomburg D., Krämer R., Burkovski A. A combination of metabolome and transcriptome analyses reveals new targets of the Corynebacterium glutamicum nitrogen regulator AmtR. J. Biotechnol. 2009, 140:68-74.
12. Bussmann M., Baumgart M., Bott M. RosR (Cg1324), a hydrogen peroxide-sensitive MarR-type transcriptional regulator of Corynebacterium glutamicum. J. Biol. Chem. 2010, 285:29305-29318.
13. Claes W.A., Pühler A., Kalinowski J. Identification of two prpDBC gene clusters in Corynebacterium glutamicum and their involvement in propionate degradation via the 2-methylcitrate cycle. J. Bacteriol. 2002, 184:2728-2739.
14. Cramer A., Auchter M., Frunzke J., Bott M., Eikmanns B.J. RamB, the transcriptional regulator of acetate metabolism in Corynebacterium glutamicum, is subject to regulation by RamA and RamB. J. Bacteriol. 2007, 189:1145-1149.
15. Cramer A., Eikmanns B.J. RamA, the transcriptional regulator of acetate metabolism in Corynebacterium glutamicum, is subject to negative autoregulation. J. Mol. Microbiol. Biotechnol. 2007, 12:51-59.
16. Cramer A., Gerstmeir R., Schaffer S., Bott M., Eikmanns B.J. Identification of RamA, a novel LuxR-type transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J. Bacteriol. 2006, 188:2554-2567.
17. Doan T., Servant P., Tojo S., Yamaguchi H., Lerondel G., Yoshida K.-I., Fujita Y., Aymerich S. The Bacillus subtilis ywkA gene encodes a malic enzyme and its transcription is activated by the YufL/YufM two-component system in response to malate. Microbiology 2003, 149:2331-2343.
18. Dominguez H., Cocaign-Bousquet M., Lindley N.D. Simultaneous consumption of glucose and fructose from sugar mixtures during batch growth of Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 1997, 47:600-603.
19. Dominguez H., Rollin C., Guyonvarch A., Guerquin-Kern J.L., Cocaign-Bousquet M., Lindley N.D. Carbon-flux distribution in the central metabolic pathways of Corynebacterium glutamicum during growth on fructose. Eur. J. Biochem. 1998, 254:96-102.
20. Eggeling L., Bott M. Handbook of Corynebacterium glutamicum 2005, Taylor & Francis, Boca Raton.
21. Engels V., Wendisch V.F. The DeoR-type regulator SugR represses expression of ptsG in Corynebacterium glutamicum. J. Bacteriol. 2007, 189:2955-2966.
22. Frunzke J., Engels V., Hasenbein S., Gätgens C., Bott M. Co-ordinated regulation of gluconate catabolism and glucose uptake in Corynebacterium glutamicum by two functionally equivalent transcriptional regulators, GntR1 and GntR2. Mol. Microbiol. 2008, 67:305-322.
23. Gaigalat L., Schlüter J.-P., Hartmann M., Mormann S., Tauch A., Pühler A., Kalinowski J. The DeoR-type transcriptional regulator SugR acts as a repressor for genes encoding the phosphoenolpyruvate:sugar phosphotransferase system (PTS) in Corynebacterium glutamicum. BMC Mol. Biol. 2007, 8:104.
24. Georgi T., Engels V., Wendisch V.F. Regulation of l-lactate utilization by the FadR-type regulator LldR of Corynebacterium glutamicum. J. Bacteriol. 2008, 190:963-971.
25. Georgi T., Rittmann D., Wendisch V.F. Lysine and glutamate production by Corynebacterium glutamicum on glucose, fructose and sucrose: roles of malic enzyme and fructose-1,6-bisphosphatase. Metab. Eng. 2005, 7:291-301.
26. Gerstmeir R., Cramer A., Dangel P., Schaffer S., Eikmanns B.J. RamB, a novel transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J. Bacteriol. 2004, 186:2798-2809.
27. Gerstmeir R., Wendisch V.F., Schnicke S., Ruan H., Farwick M., Reinscheid D., Eikmanns B.J. Acetate metabolism and its regulation in Corynebacterium glutamicum. J. Biotechnol. 2003, 104:99-122.
28. Gourdon P., Baucher M.F., Lindley N.D., Guyonvarch A. Cloning of the malic enzyme gene from Corynebacterium glutamicum and role of the enzyme in lactate metabolism. Appl. Environ. Microbiol. 2000, 66:2981-2987.
29. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 1983, 166:557-580.
30. Ikeda M., Nakagawa S. The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl. Microbiol. Biotechnol. 2003, 62:99-109.
31. Kalinowski J., Bathe B., Bartels D., Bischoff N., Bott M., Burkovski A., Dusch N., Eggeling L., Eikmanns B.J., Gaigalat L., Goesmann A., Hartmann M., Huthmacher K., Krämer R., Linke B., McHardy A.C., Meyer F., Möckel B., Pfefferle W., Pühler A., Rey D.A., Rückert C., Rupp O., Sahm H., Wendisch V.F., Wiegräbe I., Tauch A. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of l-aspartate-derived amino acids and vitamins. J. Biotechnol. 2003, 104:5-25.
32. Keilhauer C., Eggeling L., Sahm H. Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon. J. Bacteriol. 1993, 175:5595-5603.
33. Kim H.-J., Kim T.-H., Kim Y., Lee H.-S. Identification and characterization of glxR, a gene involved in regulation of glyoxylate bypass in Corynebacterium glutamicum. J. Bacteriol. 2004, 186:3453-3460.
34. Knoppová M., Phensaijai M., Veselý M., Zemanová M., Nesvera J., Pátek M. Plasmid vectors for testing in vivo promoter activities in Corynebacterium glutamicum and Rhodococcus erythropolis. Curr. Microbiol. 2007, 55:234-239.
35. Krug A., Wendisch V.F., Bott M. Identification of AcnR, a TetR-type repressor of the aconitase gene acn in Corynebacterium glutamicum. J. Biol. Chem. 2005, 280:585-595.
36. Kunst F., Ogasawara N., Moszer I., Albertini A.M., Alloni G., Azevedo V., Bertero M.G., Bessières P., Bolotin A., Borchert S., Borriss R., Boursier L., Brans A., Braun M., Brignell S.C., Bron S., Brouillet S., Bruschi C.V., Caldwell B., Capuano V., Carter N.M., Choi S.K., Codani J.J., Connerton I.F., Danchin A. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 1997, 390:249-256.
37. Laslo, T., von Zaluskowski, P., Gabris, C., Lodd, E., Rückert, C., Dangel, P., Kalinowski, J., Auchter, M., Seibold, G., Eikmanns, B.J. Arabitol metabolism of Corynebacterium glutamicum and its regulation by AtlR. J. Bacteriol., in press. doi:10.1128/%20JB.06064-11.
38. Lee H.-W., Pan J.-G., Lebeault J.-M. Enhanced l-lysine production in threonine-limited continuous culture of Corynebacterium glutamicum by using gluconate as a secondary carbon source with glucose. Appl. Microbiol. Biotechnol. 1998, 49:9-15.
39. Lerondel G., Doan T., Zamboni N., Sauer U., Aymerich S. YtsJ has the major physiological role of the four paralogous malic enzyme isoforms in Bacillus subtilis. J. Bacteriol. 2006, 188:4727-4736.
40. Lindner S.N., Niederholtmeyer H., Schmitz K., Schoberth S.M., Wendisch V.F. Polyphosphate/ATP-dependent NAD kinase of Corynebacterium glutamicum: biochemical properties and impact of ppnK overexpression on lysine production. Appl. Microbiol. Biotechnol. 2010, 87:583-593.
41. Merkens H., Beckers G., Wirtz A., Burkovski A. Vanillate metabolism in Corynebacterium glutamicum. Curr. Microbiol. 2005, 51:59-65.
42. Nentwich S.S., Brinkrolf K., Gaigalat L., Hüser A.T., Rey D.A., Mohrbach T., Marin K., Pühler A., Tauch A., Kalinowski J. Characterization of the LacI-type transcriptional repressor RbsR controlling ribose transport in Corynebacterium glutamicum ATCC 13032. Microbiology 2009, 155:150-164.
43. Netzer R., Krause M., Rittmann D., Peters-Wendisch P.G., Eggeling L., Wendisch V.F., Sahm H. Roles of pyruvate kinase and malic enzyme in Corynebacterium glutamicum for growth on carbon sources requiring gluconeogenesis. Arch. Microbiol. 2004, 182:354-363.
44. Netzer R., Peters-Wendisch P., Eggeling L., Sahm H. Cometabolism of a nongrowth substrate: l-serine utilization by Corynebacterium glutamicum. Appl. Environ. Microbiol. 2004, 70:7148-7155.
45. Neuner A., Heinzle E. Mixed glucose and lactate uptake by Corynebacterium glutamicum through metabolic engineering. Biotechnol. J. 2011, 6:318-329.
46. Niebisch A., Bott M. Molecular analysis of the cytochrome bc1-aa3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c1. Arch. Microbiol. 2001, 175:282-294.
47. Oh M.-K., Rohlin L., Kao K.C., Liao J.C. Global expression profiling of acetate-grown Escherichia coli. J. Biol. Chem. 2002, 277:13175-13183.
48. Pátek M., Nesvera J., Guyonvarch A., Reyes O., Leblon G. Promoters of Corynebacterium glutamicum. J. Biotechnol. 2003, 104:311-323.
49. Pérez-Rueda E., Collado-Vides J. Common history at the origin of the position-function correlation in transcriptional regulators in archaea and bacteria. J. Mol. Evol. 2001, 53:172-179.
50. Petersen S., de Graaf A.A., Eggeling L., Möllney M., Wiechert W., Sahm H. In vivo quantification of parallel and bidirectional fluxes in the anaplerosis of Corynebacterium glutamicum. J. Biol. Chem. 2000, 275:35932-35941.
51. Peters-Wendisch P.G., Schiel B., Wendisch V.F., Katsoulidis E., Möckel B., Sahm H., Eikmanns B.J. Pyruvate carboxylase is a major bottleneck for glutamate and lysine production by Corynebacterium glutamicum. J. Mol. Microbiol. Biotechnol. 2001, 3:295-300.
52. Polen T., Schluesener D., Poetsch A., Bott M., Wendisch V.F. Characterization of citrate utilization in Corynebacterium glutamicum by transcriptome and proteome analysis. FEMS Microbiol. Lett. 2007, 273:109-119.
53. Riedel C., Rittmann D., Dangel P., Möckel B., Petersen S., Sahm H., Eikmanns B.J. Characterization of the phosphoenolpyruvate carboxykinase gene from Corynebacterium glutamicum and significance of the enzyme for growth and amino acid production. J. Mol. Microbiol. Biotechnol. 2001, 3:573-583.
54. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor laboratory Press, Cold Spring Harbor.
55. Sassetti C.M., Rubin E.J. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. U.S.A 2003, 100:12989-12994.
56. Sauer U., Eikmanns B.J. The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. FEMS Microbiol. Rev. 2005, 29:765-794.
57. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 1994, 145:69-73.
58. Schaffer S., Weil B., Nguyen V.D., Dongmann G., Günther K., Nickolaus M., Hermann T., Bott M. A high-resolution reference map for cytoplasmic and membrane-associated proteins of Corynebacterium glutamicum. Electrophoresis 2001, 22:4404-4422.
59. Stansen C., Uy D., Delaunay S., Eggeling L., Goergen J.-L., Wendisch V.F. Characterization of a Corynebacterium glutamicum lactate utilization operon induced during temperature-triggered glutamate production. Appl. Environ. Microbiol. 2005, 71:5920-5928.
60. Tanaka Y., Okai N., Teramoto H., Inui M., Yukawa H. Regulation of the expression of phosphoenolpyruvate: carbohydrate phosphotransferase system (PTS) genes in Corynebacterium glutamicum R. Microbiology 2008, 154:264-274.
61. van der Rest M.E., Frank C., Molenaar D. Functions of the membrane-associated and cytoplasmic malate dehydrogenases in the citric acid cycle of Escherichia coli. J. Bacteriol. 2000, 182:6892-6899.
62. van der Rest M.E., Lange C., Molenaar D. A heat shock following electroporation induces highly efficient transformation of Corynebacterium glutamicum with xenogeneic plasmid DNA. Appl. Microbiol. Biotechnol. 1999, 52:541-545.
63. Wendisch V.F., de Graaf A.A., Sahm H., Eikmanns B.J. Quantitative determination of metabolic fluxes during coutilization of two carbon sources: comparative analyses with Corynebacterium glutamicum during growth on acetate and/or glucose. J. Bacteriol. 2000, 182:3088-3096.
64. Wennerhold J., Krug A., Bott M. The AraC-type regulator RipA represses aconitase and other iron proteins from Corynebacterium under iron limitation and is itself repressed by DtxR. J. Biol. Chem. 2005, 280:40500-40508.
65. Wilkinson S.P., Grove A. Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Curr. Issues Mol. Biol. 2006, 8:51-62.
66. Youn J.-W., Jolkver E., Krämer R., Marin K., Wendisch V.F. Identification and characterization of the dicarboxylate uptake system DccT in Corynebacterium glutamicum. J. Bacteriol. 2008, 190:6458-6466.
67. Youn J.-W., Jolkver E., Krämer R., Marin K., Wendisch V.F. Characterization of the dicarboxylate transporter DctA in Corynebacterium glutamicum. J. Bacteriol. 2009, 191:5480-5488.