Regulons of global transcription factors in Corynebacterium glutamicum

Applied Microbiology and Biotechnology volume 100, pages45–60(2016)Cite this article

Abstract

Corynebacterium glutamicum, a high GC content gram-positive soil bacterium in Actinobacteria, has been used for the industrial production of amino acids and engineered to produce various compounds, including polymer building blocks and biofuels. Since its genome sequence was first published, its versatile metabolic pathways and their genetic components and regulatory mechanisms have been extensively studied. Previous studies on transcriptional factors, including two-component systems and σ factors, in the bacterium have revealed transcriptional regulatory links among the metabolic pathways and those among the stress response systems, forming a complex transcriptional regulatory network. The regulatory links are based on knowledge of the transcription factors, such as their target genes (regulons), DNA sequence motifs for recognition, and effector molecules controlling their activities, all of which are fundamental for understanding their physiological functions. Recent advances in chromatin immunoprecipitation (ChIP)-based genome-wide analyses provide an opportunity to comprehensively identify the transcription factor regulon, composed of its direct target genes, and its precise consensus binding motif. A common feature among the regulon constituents may provide clues to identify an effector molecule targeting the factor. In this mini-review, we summarize the current knowledge of the regulons of the C. glutamicum transcription factors that have been analyzed via ChIP-based technologies. The regulons consisting of direct target genes revealed new physiological roles of the transcription factors and new regulatory interactions, contributing to refinement and expansion of the transcriptional regulatory network and the development of guidelines and genetic tools for metabolic engineering of C. glutamicum.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Arndt A, Eikmanns BJ (2007) The alcohol dehydrogenase gene adhA in Corynebacterium glutamicum is subject to carbon catabolite repression. J Bacteriol 189:7408–7416

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  2. Auchter M, Arndt A, Eikmanns BJ (2009) Dual transcriptional control of the acetaldehyde dehydrogenase gene ald of Corynebacterium glutamicum by RamA and RamB. J Biotechnol 140:84–91

    PubMed  CAS  Article  Google Scholar 

  3. Auchter M, Cramer A, Hüser A, Rückert C, Emer D, Schwarz P, Arndt A, Lange C, Kalinowski J, Wendisch VF, Eikmanns BJ (2011a) RamA and RamB are global transcriptional regulators in Corynebacterium glutamicum and control genes for enzymes of the central metabolism. J Biotechnol 154:126–139

    PubMed  CAS  Article  Google Scholar 

  4. Auchter M, Laslo T, Fleischer C, Schiller L, Arndt A, Gaigalat L, Kalinowski J, Eikmanns BJ (2011b) Control of adhA and sucR expression by the SucR regulator in Corynebacterium glutamicum. J Biotechnol 152:77–86

    PubMed  CAS  Article  Google Scholar 

  5. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymer. Proc Int Conf Intell Syst Mol Biol 2:28–36

    PubMed  CAS  Google Scholar 

  6. Barreiro C, González-Lavado E, Pátek M, Martin JF (2004) Transcriptional analysis of the groES-groEL1, groEL2, and dnaK genes in Corynebacterium glutamicum: characterization of heat shock-induced promoters. J Bacteriol 186:4813–4817

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  7. Baumbach J, Brinkrolf K, Czaja LF, Rahmann S, Tauch A (2006) CoryneRegNet: an ontology-based data warehouse of corynebacterial transcription factors and regulatory networks. BMC Genomics 7:24

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  8. Baumbach J, Wittkop T, Rademacher K, Rahmann S, Brinkrolf K, Tauch A (2007) CoryneRegNet 3.0--an interactive systems biology platform for the analysis of gene regulatory networks in corynebacteria and Escherichia coli. J Biotechnol 129:279–289

    PubMed  CAS  Article  Google Scholar 

  9. Becker J, Wittmann C (2012) Bio-based production of chemicals, materials and fuels -Corynebacterium glutamicum as versatile cell factory. Curr Opin Biotechnol 23:631–640

    PubMed  CAS  Article  Google Scholar 

  10. Becker J, Klopprogge C, Herold A, Zelder O, Bolten CJ, Wittmann C (2007) Metabolic flux engineering of L-lysine production in Corynebacterium glutamicum--over expression and modification of G6P dehydrogenase. J Biotechnol 132:99–109

    PubMed  CAS  Article  Google Scholar 

  11. Bott M (2007) Offering surprises: TCA cycle regulation in Corynebacterium glutamicum. Trends Microbiol 15:417–425

    PubMed  CAS  Article  Google Scholar 

  12. Bott M, Brocker M (2012) Two-component signal transduction in Corynebacterium glutamicum and other corynebacteria: on the way towards stimuli and targets. Appl Microbiol Biotechnol 94:1131–1150

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  13. Brinkman AB, Ettema TJG, de Vos WM, van der Oost J (2003) The Lrp family of transcriptional regulators. Mol Microbiol 48:287–294

    PubMed  CAS  Article  Google Scholar 

  14. Brinkrolf K, Brune I, Tauch A (2006) Transcriptional regulation of catabolic pathways for aromatic compounds in Corynebacterium glutamicum. Genet Mol Res 5:773–789

    PubMed  Google Scholar 

  15. Brinkrolf K, Brune I, Tauch A (2007) The transcriptional regulatory network of the amino acid producer Corynebacterium glutamicum. J Biotechnol 129:191–211

    PubMed  CAS  Article  Google Scholar 

  16. Brinkrolf K, Schröder J, Pühler A, Tauch A (2010) The transcriptional regulatory repertoire of Corynebacterium glutamicum: reconstruction of the network controlling pathways involved in lysine and glutamate production. J Biotechnol 149:173–182

    PubMed  CAS  Article  Google Scholar 

  17. Brocker M, Bott M (2006) Evidence for activator and repressor functions of the response regulator MtrA from Corynebacterium glutamicum. FEMS Microbiol Lett 264:205–212

    PubMed  CAS  Article  Google Scholar 

  18. Brocker M, Schaffer S, Mack C, Bott M (2009) Citrate utilization by Corynebacterium glutamicum is controlled by the CitAB two-component system through positive regulation of the citrate transport genes citH and tctCBA. J Bacteriol 191:3869–3880

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  19. Brocker M, Mack C, Bott M (2011) Target genes, consensus binding site, and role of phosphorylation for the response regulator MtrA of Corynebacterium glutamicum. J Bacteriol 193:1237–1249

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  20. Brune I, Brinkrolf K, Kalinowski J, Pühler A, Tauch A (2005) The individual and common repertoire of DNA-binding transcriptional regulators of Corynebacterium glutamicum, Corynebacterium efficiens, Corynebacterium diphtheriae and Corynebacterium jeikeium deduced from the complete genome sequences. BMC Genomics 6:86

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  21. Brune I, Werner H, Huser AT, Kalinowski J, Pühler A, Tauch A (2006) The DtxR protein acting as dual transcriptional regulator directs a global regulatory network involved in iron metabolism of Corynebacterium glutamicum. BMC Genomics 7:21

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  22. Bucca G, Laing E, Mersinias V, Allenby N, Hurd D, Holdstock J, Brenner V, Harrison M, Smith CP (2009) Development and application of versatile high density microarrays for genome-wide analysis of Streptomyces coelicolor: characterization of the HspR regulon. Genome Biol 10:R5

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. Busche T, Šilar R, Pičmanová M, Pátek M, Kalinowski J (2012) Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics 13:445

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  24. Bussmann M, Emer D, Hasenbein S, Degraf S, Eikmanns BJ, Bott M (2009) Transcriptional control of the succinate dehydrogenase operon sdhCAB of Corynebacterium glutamicum by the cAMP-dependent regulator GlxR and the LuxR-type regulator RamA. J Biotechnol 143:173–182

    PubMed  CAS  Article  Google Scholar 

  25. Cha PH, Park SY, Moon MW, Subhadra B, Oh TK, Kim E, Kim JF, Lee JK (2010) Characterization of an adenylate cyclase gene (cyaB) deletion mutant of Corynebacterium glutamicum ATCC 13032. Appl Microbiol Biotechnol 85:1061–1068

    PubMed  CAS  Article  Google Scholar 

  26. Chao H, Zhou NY (2013) GenR, an IclR-type regulator, activates and represses the transcription of gen genes involved in 3-hydroxybenzoate and gentisate catabolism in Corynebacterium glutamicum. J Bacteriol 195:1598–1609

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  27. Chao H, Zhou NY (2014) Involvement of the global regulator GlxR in 3-hydroxybenzoate and gentisate utilization by Corynebacterium glutamicum. Appl Environ Microbiol 80:4215–4225

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  28. Cho BK, Barrett CL, Knight EM, Park YS, Palsson BO (2008) Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli. Proc Natl Acad Sci U S A 105:19462–19467

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  29. Cho HY, Lee SG, Hyeon JE, Han SO (2010) Identification and characterization of a transcriptional regulator, SucR, that influences sucCD transcription in Corynebacterium glutamicum. Biochem Biophys Res Commun 401:300–300–305

    PubMed  CAS  Article  Google Scholar 

  30. Choi WW, Park SD, Lee SM, Kim HB, Kim Y, Lee HS (2009) The whcA gene plays a negative role in oxidative stress response of Corynebacterium glutamicum. FEMS Microbiol Lett 290:32–38

    PubMed  CAS  Article  Google Scholar 

  31. Cocaign-Bousquet M, Monnet C, Lindley ND (1993) Batch kinetics of Corynebacterium glutamicum during growth on various carbon substrates: use of substrate mixtures to localise metabolic bottlenecks. Appl Microbiol Biotechnol 40:526–530

    Google Scholar 

  32. Cramer A, Eikmanns BJ (2007) RamA, the transcriptional regulator of acetate metabolism in Corynebacterium glutamicum, is subject to negative autoregulation. J Mol Microbiol Biotechnol 12:51–59

    PubMed  CAS  Article  Google Scholar 

  33. Cramer A, Gerstmeir R, Schaffer S, Bott M, Eikmanns BJ (2006) Identification of RamA, a novel LuxR-type transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol 188:2554–2567

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  34. Cramer A, Auchter M, Frunzke J, Bott M, Eikmanns BJ (2007) RamB, the transcriptional regulator of acetate metabolism in Corynebacterium glutamicum, is subject to regulation by RamA and RamB. J Bacteriol 189:1145–1149

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  35. Dietrich C, Nato A, Bost B, Le Marechal P, Guyonvarch A (2009) Regulation of ldh expression during biotin-limited growth of Corynebacterium glutamicum. Microbiology 155:1360–1375

    PubMed  CAS  Article  Google Scholar 

  36. Dominguez H, Lindley ND (1996) Complete sucrose metabolism requires fructose phosphotransferase activity in Corynebacterium glutamicum to ensure phosphorylation of liberated fructose. Appl Environ Microbiol 62:3878–3880

    PubMed  CAS  PubMed Central  Google Scholar 

  37. Dominguez H, Cocaign-Bousquet M, Lindley ND (1997) Simultaneous consumption of glucose and fructose from sugar mixtures during batch growth of Corynebacterium glultamicum. Appl Microbiol Biotechnol 47:600–603

    CAS  Article  Google Scholar 

  38. Dominguez H, Rollin C, Guyonvarch A, Guerquin-Kern JL, Cocaign-Bousquet M, Lindley ND (1998) Carbon-flux distribution in the central metabolic pathways of Corynebacterium glutamicum during growth on fructose. Eur J Biochem 254:96–102

    PubMed  CAS  Article  Google Scholar 

  39. Ehira S, Shirai T, Teramoto H, Inui M, Yukawa H (2008) Group 2 sigma factor SigB of Corynebacterium glutamicum positively regulates glucose metabolism under conditions of oxygen deprivation. Appl Environ Microbiol 74:5146–5152

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  40. Ehira S, Ogino H, Teramoto H, Inui M, Yukawa H (2009a) Regulation of quinone oxidoreductase by the redox-sensing transcriptional regulator QorR in Corynebacterium glutamicum. J Biol Chem 284:16736–16742

  41. Ehira S, Teramoto H, Inui M, Yukawa H (2009b) Regulation of Corynebacterium glutamicum heat shock response by the extracytoplasmic-function sigma factor SigH and transcriptional regulators HspR and HrcA. J Bacteriol 191:2964–2972

  42. Emer D, Krug A, Eikmanns BJ, Bott M (2009) Complex expression control of the Corynebacterium glutamicum aconitase gene: identification of RamA as a third transcriptional regulator besides AcnR and RipA. J Biotechnol 140:92–98

    PubMed  CAS  Article  Google Scholar 

  43. Engels V, Wendisch VF (2007) The DeoR-Type regulator SugR represses expression of ptsG in Corynebacterium glutamicum. J Bacteriol 189:2955–2966

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  44. Engels S, Schweitzer JE, Ludwig C, Bott M, Schaffer S (2004) clpC and clpP1P2 gene expression in Corynebacterium glutamicum is controlled by a regulatory network involving the transcriptional regulators ClgR and HspR as well as the ECF sigma factor σH. Mol Microbiol 52:285–302

    PubMed  CAS  Article  Google Scholar 

  45. Engels S, Ludwig C, Schweitzer JE, Mack C, Bott M, Schaffer S (2005) The transcriptional activator ClgR controls transcription of genes involved in proteolysis and DNA repair in Corynebacterium glutamicum. Mol Microbiol 57:576–591

    PubMed  CAS  Article  Google Scholar 

  46. Engels V, Georgi T, Wendisch VF (2008a) ScrB (Cg2927) is a sucrose-6-phosphate hydrolase essential for sucrose utilization by Corynebacterium glutamicum. FEMS Microbiol Lett 289:80–89

    PubMed  CAS  Article  Google Scholar 

  47. Engels V, Lindner SN, Wendisch VF (2008b) The global repressor SugR controls expression of genes of glycolysis and of the L-lactate dehydrogenase LdhA in Corynebacterium glutamicum. J Bacteriol 190:8033–8044

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  48. Frunzke J, Engels V, Hasenbein S, Gatgens C, Bott M (2008) Co-ordinated regulation of gluconate catabolism and glucose uptake in Corynebacterium glutamicum by two functionally equivalent transcriptional regulators, GntR1 and GntR2. Mol Microbiol 67:305–322

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  49. Frunzke J, Gatgens C, Brocker M, Bott M (2011) Control of heme homeostasis in Corynebacterium glutamicum by the two-component system HrrSA. J Bacteriol 193:1212–1221

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  50. Fujita Y, Miwa Y (1989) Identification of an operator sequence for the Bacillus subtilis gnt operon. J Biol Chem 264:4201–4206

    PubMed  CAS  Google Scholar 

  51. Furusawa C, Horinouchi T, Hirasawa T, Shimizu H (2013) Systems metabolic engineering: the creation of microbial cell factories by rational metabolic design and evolution. Adv Biochem Eng Biotechnol 131:1–23

    PubMed  CAS  Google Scholar 

  52. Gaigalat L, Schlueter JP, Hartmann M, Mormann S, Tauch A, Pühler A, Kalinowski J (2007) 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 8:104

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  53. Galagan J, Lyubetskaya A, Gomes A (2013a) ChIP-Seq and the complexity of bacterial transcriptional regulation. Curr Top Microbiol Immunol 363:43–68

    PubMed  CAS  Google Scholar 

  54. Galagan JE, Minch K, Peterson M, Lyubetskaya A, Azizi E, Sweet L, Gomes A, Rustad T, Dolganov G, Glotova I, Abeel T, Mahwinney C, Kennedy AD, Allard R, Brabant W, Krueger A, Jaini S, Honda B, Yu WH, Hickey MJ, Zucker J, Garay C, Weiner B, Sisk P, Stolte C, Winkler JK, Van de Peer Y, Iazzetti P, Camacho D, Dreyfuss J, Liu Y, Dorhoi A, Mollenkopf HJ, Drogaris P, Lamontagne J, Zhou Y, Piquenot J, Park ST, Raman S, Kaufmann SH, Mohney RP, Chelsky D, Moody DB, Sherman DR, Schoolnik GK (2013b) The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499:178–183

  55. Gao Y-G, Suzuki H, Itou H, Zhou Y, Tanaka Y, Wachi M, Watanabe N, Tanaka I, Yao M (2008) Structural and functional characterization of the LldR from Corynebacterium glutamicum: a transcriptional repressor involved in L-lactate and sugar utilization. Nucleic Acids Res 36:7110–7123

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  56. Georgi T, Engels V, Wendisch VF (2008) Regulation of L-lactate utilization by the FadR-type regulator LldR of Corynebacterium glutamicum. J Bacteriol 190:963–971

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  57. Gerstmeir R, Wendisch VF, Schnicke S, Ruan H, Farwick M, Reinscheid D, Eikmanns BJ (2003) Acetate metabolism and its regulation in Corynebacterium glutamicum. J Biotechnol 104:99–122

    PubMed  CAS  Article  Google Scholar 

  58. Gerstmeir R, Cramer A, Dangel P, Schaffer S, Eikmanns BJ (2004) RamB, a novel transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol 186:2798–2809

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  59. Grainger DC, Busby SJ (2008) Methods for studying global patterns of DNA binding by bacterial transcription factors and RNA polymerase. Biochem Soc Trans 36:754–757

    PubMed  CAS  Article  Google Scholar 

  60. Grainger DC, Overton TW, Reppas N, Wade JT, Tamai E, Hobman JL, Constantinidou C, Struhl K, Church G, Busby SJW (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186:6938–6943

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  61. Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJW (2005) Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci U S A 102:17693–17698

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  62. Grainger DC, Aiba H, Hurd D, Browning DF, Busby SJ (2007) Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res 35:269–278

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  63. Grainger DC, Lee DJ, Busby SJ (2009) Direct methods for studying transcription regulatory proteins and RNA polymerase in bacteria. Curr Opin Microbiol 12:531–535

    PubMed  CAS  Article  Google Scholar 

  64. Han SO, Inui M, Yukawa H (2007) Expression of Corynebacterium glutamicum glycolytic genes varies with carbon source and growth phase. Microbiology 153:2190–2202

    PubMed  CAS  Article  Google Scholar 

  65. Han SO, Inui M, Yukawa H (2008) Effect of carbon source availability and growth phase on expression of Corynebacterium glutamicum genes involved in the tricarboxylic acid cycle and glyoxylate bypass. Microbiology 154:3073–3083

    PubMed  CAS  Article  Google Scholar 

  66. Hansmeier N, Albersmeier A, Tauch A, Damberg T, Ros R, Anselmetti D, Pühler A, Kalinowski J (2006) The surface (S)-layer gene cspB of Corynebacterium glutamicum is transcriptionally activated by a LuxR-type regulator and located on a 6 kb genomic island absent from the type strain ATCC 13032. Microbiology 152:923–935

    PubMed  CAS  Article  Google Scholar 

  67. Hayashi M, Mizoguchi H, Shiraishi N, Obayashi M, Nakagawa S, Imai J, Watanabe S, Ota T, Ikeda M (2002) Transcriptome analysis of acetate metabolism in Corynebacterium glutamicum using a newly developed metabolic array. Biosci Biotechnol Biochem 66:1337–1344

    PubMed  CAS  Article  Google Scholar 

  68. Helmann JD (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110

    PubMed  CAS  Article  Google Scholar 

  69. Henrich A, Kuhlmann N, Eck AW, Krämer R, Seibold GM (2013) Maltose uptake by the novel ABC transport system MusEFGK2I causes increased expression of ptsG in Corynebacterium glutamicum. J Bacteriol 195:2573–2584

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  70. Hentschel E, Mack C, Gätgens C, Bott M, Brocker M, Frunzke J (2014) Phosphatase activity of the histidine kinases ensures pathway specificity of the ChrSA and HrrSA two-component systems in Corynebacterium glutamicum. Mol Microbiol 92:1326–1342

    PubMed  CAS  Article  Google Scholar 

  71. Hermann T (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155–172

    PubMed  CAS  Article  Google Scholar 

  72. Heyer A, Gatgens C, Hentschel E, Kalinowski J, Bott M, Frunzke J (2012) The two-component system ChrSA is crucial for haem tolerance and interferes with HrrSA in haem-dependent gene regulation in Corynebacterium glutamicum. Microbiology 158:3020–3031

    PubMed  CAS  Article  Google Scholar 

  73. Hirasawa T, Kim J, Shirai T, Furusawa C, Shimizu H (2012) Molecular mechanisms and metabolic engineering of glutamate overproduction in Corynebacterium glutamicum. Subcell Biochem 64:261–281

    PubMed  CAS  Article  Google Scholar 

  74. Ikeda M (2003) Amino acid production processes. Adv Biochem Eng Biotechnol 79:1–35

    PubMed  CAS  Google Scholar 

  75. Ikeda M, Nakagawa S (2003) The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol 62:99–109

    PubMed  CAS  Article  Google Scholar 

  76. Inui M, Suda M, Okino S, Nonaka H, Puskás LG, Vertès AA, Yukawa H (2007) Transcriptional profiling of Corynebacterium glutamicum metabolism during organic acid production under oxygen deprivation conditions. Microbiology 153:2491–2504

    PubMed  CAS  Article  Google Scholar 

  77. Izu H, Adachi O, Yamada M (1997) Gene organization and transcriptional regulation of the gntRKU operon involved in gluconate uptake and catabolism of Escherichia coli. J Mol Biol 267:778–793

    PubMed  CAS  Article  Google Scholar 

  78. Jojima T, Noburyu R, Sasaki M, Tajima T, Suda M, Yukawa H, Inui M (2015) Metabolic engineering for improved production of ethanol by Corynebacterium glutamicum. Appl Microbiol Biotechnol 99:1165–1172

    PubMed  CAS  Article  Google Scholar 

  79. Jolkver E, Emer D, Ballan S, Krämer R, Eikmanns BJ, Marin K (2009) Identification and characterization of a bacterial transport system for the uptake of pyruvate, propionate, and acetate in Corynebacterium glutamicum. J Bacteriol 191:940–948

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  80. Jungwirth B, Emer D, Brune I, Hansmeier N, Pühler A, Eikmanns BJ, Tauch A (2008) Triple transcriptional control of the resuscitation promoting factor 2 (rpf2) gene of Corynebacterium glutamicum by the regulators of acetate metabolism RamA and RamB and the cAMP-dependent regulator GlxR. FEMS Microbiol Lett 281:190–197

    PubMed  CAS  Article  Google Scholar 

  81. Jungwirth B, Sala C, Kohl TA, Uplekar S, Baumbach J, Cole ST, Pühler A, Tauch A (2013) High-resolution detection of DNA binding sites of the global transcriptional regulator GlxR in Corynebacterium glutamicum. Microbiology 159:12–22

    PubMed  CAS  Article  Google Scholar 

  82. Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, Goesmann A, Hartmann M, Huthmacher K, Kramer R, Linke B, McHardy AC, Meyer F, Mockel B, Pfefferle W, Pühler A, Rey DA, Ruckert C, Rupp O, Sahm H, Wendisch VF, Wiegrabe I, Tauch A (2003) The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol 104:5–25

    PubMed  CAS  Article  Google Scholar 

  83. Kiefer P, Heinzle E, Zelder O, Wittmann C (2004) Comparative metabolic flux analysis of lysine-producing Corynebacterium glutamicum cultured on glucose or fructose. Appl Environ Microbiol 70:229–239

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  84. Kim HJ, Kim TH, Kim Y, Lee HS (2004) Identification and characterization of glxR, a gene involved in regulation of glyoxylate bypass in Corynebacterium glutamicum. J Bacteriol 186:3453–3460

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  85. Kim TH, Kim HJ, Park JS, Kim Y, Kim P, Lee HS (2005a) Functional analysis of sigH expression in Corynebacterium glutamicum. Biochem Biophys Res Commun 331:1542–1547

    PubMed  CAS  Article  Google Scholar 

  86. Kim TH, Park JS, Kim HJ, Kim Y, Kim P, Lee HS (2005b) The whcE gene of Corynebacterium glutamicum is important for survival following heat and oxidative stress. Biochem Biophys Res Commun 337:757–764

    PubMed  CAS  Article  Google Scholar 

  87. Kim MS, Dufour YS, Yoo JS, Cho YB, Park JH, Nam GB, Kim HM, Lee KL, Donohue TJ, Roe JH (2012) Conservation of thiol-oxidative stress responses regulated by SigR orthologues in actinomycetes. Mol Microbiol 85:326–344

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  88. Kind S, Neubauer S, Becker J, Yamamoto M, Volkert M, Abendroth G, Zelder O, Wittmann C (2014) From zero to hero—production of bio-based nylon from renewable resources using engineered Corynebacterium glutamicum. Metab Eng 25:113–123

    PubMed  CAS  Article  Google Scholar 

  89. Klaffl S, Brocker M, Kalinowski J, Eikmanns BJ, Bott M (2013) Complex regulation of the phosphoenolpyruvate carboxykinase gene pck and characterization of its GntR-type regulator IolR as a repressor of myo-inositol utilization genes in Corynebacterium glutamicum. J Bacteriol 195:4283–4296

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  90. Koch DJ, Ruckert C, Albersmeier A, Huser AT, Tauch A, Pühler A, Kalinowski J (2005) The transcriptional regulator SsuR activates expression of the Corynebacterium glutamicum sulphonate utilization genes in the absence of sulphate. Mol Microbiol 58:480–494

    PubMed  CAS  Article  Google Scholar 

  91. Kohl TA, Tauch A (2009) The GlxR regulon of the amino acid producer Corynebacterium glutamicum: detection of the corynebacterial core regulon and integration into the transcriptional regulatory network model. J Biotechnol 143:239–246

    PubMed  CAS  Article  Google Scholar 

  92. Kohl TA, Baumbach J, Jungwirth B, Pühler A, Tauch A (2008) The GlxR regulon of the amino acid producer Corynebacterium glutamicum: In silico and in vitro detection of DNA binding sites of a global transcription regulator. J Biotechnol 135:340–350

    PubMed  CAS  Article  Google Scholar 

  93. Kolb A, Busby S, Buc H, Garges S, Adhya S (1993) Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62:749–795

    PubMed  CAS  Article  Google Scholar 

  94. Kotrbova-Kozak A, Kotrba P, Inui M, Sajdok J, Yukawa H (2007) Transcriptionally regulated adhA gene encodes alcohol dehydrogenase required for ethanol and n-propanol utilization in Corynebacterium glutamicum R. Appl Microbiol Biotechnol 76:1347–1356

  95. Krause JP, Polen T, Youn JW, Emer D, Eikmanns BJ, Wendisch VF (2012) Regulation of the malic enzyme gene malE by the transcriptional regulator MalR in Corynebacterium glutamicum. J Biotechnol 159:204–215

    PubMed  CAS  Article  Google Scholar 

  96. Krin E, Sismeiro O, Danchin A, Bertin PN (2002) The regulation of Enzyme IIAGlc expression controls adenylate cyclase activity in Escherichia coli. Microbiology 148:1553–1559

    PubMed  CAS  Article  Google Scholar 

  97. Kronemeyer W, Peekhaus N, Krämer R, Sahm H, Eggeling L (1995) Structure of the gluABCD cluster encoding the glutamate uptake system of Corynebacterium glutamicum. J Bacteriol 177:1152–1158

    PubMed  CAS  PubMed Central  Google Scholar 

  98. Krug A, Wendisch VF, Bott M (2005) Identification of AcnR, a TetR-type repressor of the aconitase gene acn in Corynebacterium glutamicum. J Biol Chem 280:585–595

    PubMed  CAS  Article  Google Scholar 

  99. Lange C, Mustafi N, Frunzke J, Kennerknecht N, Wessel M, Bott M, Wendisch VF (2012) Lrp of Corynebacterium glutamicum controls expression of the brnFE operon encoding the export system for L-methionine and branched-chain amino acids. J Biotechnol 158:231–241

    PubMed  CAS  Article  Google Scholar 

  100. Laslo T, von Zaluskowski P, Gabris C, Lodd E, Rückert C, Dangel P, Kalinowski J, Auchter M, Seibold G, Eikmanns BJ (2012) Arabitol metabolism of Corynebacterium glutamicum and its regulation by AtlR. J Bacteriol 194:941–955

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  101. Laub MT, Chen SL, Shapiro L, McAdams HH (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci U S A 99:4632–4637

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  102. Lee JY, Kim HJ, Kim ES, Kim P, Kim Y, Lee HS (2013) Regulatory interaction of the Corynebacterium glutamicum whc genes in oxidative stress responses. J Biotechnol 168:149–154

    PubMed  CAS  Article  Google Scholar 

  103. Letek M, Valbuena N, Ramos A, Ordóñez E, Gil JA, Mateos LM (2006) Characterization and use of catabolite-repressed promoters from gluconate genes in Corynebacterium glutamicum. J Bacteriol 188:409–423

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  104. Lonetto MA, Brown KL, Rudd KE, Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A 91:7573–7577

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  105. Madan Babu M, Teichmann SA (2003) Functional determinants of transcription factors in Escherichia coli: protein families and binding sites. Trends Genet 19:75–79

    PubMed  CAS  Article  Google Scholar 

  106. Mangan S, Zaslaver A, Alon U (2003) The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J Mol Biol 334:197–204

    PubMed  CAS  Article  Google Scholar 

  107. Mangan S, Itzkovitz S, Zaslaver A, Alon U (2006) The incoherent feed-forward loop accelerates the response-time of the gal system of Escherichia coli. J Mol Biol 356:1073–1081

    PubMed  CAS  Article  Google Scholar 

  108. Mentz A, Neshat A, Pfeifer-Sancar K, Pühler A, Rückert C, Kalinowski J (2013) Comprehensive discovery and characterization of small RNAs in Corynebacterium glutamicum ATCC 13032. BMC Genomics 14:714

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  109. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U (2002) Network motifs: simple building blocks of complex networks. Science 298:824–827

    PubMed  CAS  Article  Google Scholar 

  110. Miwa Y, Fujita Y (1988) Purification and characterization of a repressor for the Bacillus subtilis gnt operon. J Biol Chem 263:13252–13257

    PubMed  CAS  Google Scholar 

  111. Möker N, Brocker M, Schaffer S, Krämer R, Morbach S, Bott M (2004) Deletion of the genes encoding the MtrA-MtrB two-component system of Corynebacterium glutamicum has a strong influence on cell morphology, antibiotics susceptibility and expression of genes involved in osmoprotection. Mol Microbiol 54:420–438

    PubMed  Article  CAS  Google Scholar 

  112. Moon MW, Kim HJ, Oh TK, Shin CS, Lee JS, Kim SJ, Lee JK (2005) Analyses of enzyme II gene mutants for sugar transport and heterologous expression of fructokinase gene in Corynebacterium glutamicum ATCC 13032. FEMS Microbiol Lett 244:259–266

    PubMed  CAS  Article  Google Scholar 

  113. Moon MW, Park SY, Choi SK, Lee JK (2007) The phosphotransferase system of Corynebacterium glutamicum: features of sugar transport and carbon regulation. J Mol Microbiol Biotechnol 12:43–50

    PubMed  CAS  Article  Google Scholar 

  114. Muffler A, Bettermann S, Haushalter M, Horlein A, Neveling U, Schramm M, Sorgenfrei O (2002) Genome-wide transcription profiling of Corynebacterium glutamicum after heat shock and during growth on acetate and glucose. J Biotechnol 98:255–268

    PubMed  CAS  Article  Google Scholar 

  115. Nakunst D, Larisch C, Hüser AT, Tauch A, Pühler A, Kalinowski J (2007) The extracytoplasmic function-type sigma factor SigM of Corynebacterium glutamicum ATCC 13032 is involved in transcription of disulfide stress-related genes. J Bacteriol 189:4696–4707

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  116. Nantapong N, Kugimiya Y, Toyama H, Adachi O, Matsushita K (2004) Effect of NADH dehydrogenase-disruption and over-expression on respiration-related metabolism in Corynebacterium glutamicum KY9714. Appl Microbiol Biotechnol 66:187–193

    PubMed  CAS  Article  Google Scholar 

  117. Neshat A, Mentz A, Rückert C, Kalinowski J (2014) Transcriptome sequencing revealed the transcriptional organization at ribosome-mediated attenuation sites in Corynebacterium glutamicum and identified a novel attenuator involved in aromatic amino acid biosynthesis. J Biotechnol 190:55–63

    PubMed  CAS  Article  Google Scholar 

  118. Nešvera J, Pátek M (2011) Tools for genetic manipulations in Corynebacterium glutamicum and their applications. Appl Microbiol Biotechnol 90:1641–1654

  119. Nishimura T, Teramoto H, Toyoda K, Inui M, Yukawa H (2011) Regulation of the nitrate reductase operon narKGHJI by the cAMP-dependent regulator GlxR in Corynebacterium glutamicum. Microbiology 157:21–28

    PubMed  CAS  Article  Google Scholar 

  120. Nishio Y, Nakamura Y, Kawarabayasi Y, Usuda Y, Kimura E, Sugimoto S, Matsui K, Yamagishi A, Kikuchi H, Ikeo K, Gojobori T (2003) Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res 13:1572–1579

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  121. Omumasaba CA, Okai N, Inui M, Yukawa H (2004) Corynebacterium glutamicum glyceraldehyde-3-phosphate dehydrogenase isoforms with opposite, ATP-dependent regulation. J Mol Microbiol Biotechnol 8:91–103

    PubMed  CAS  Article  Google Scholar 

  122. Panhorst M, Sorger-Herrmann U, Wendisch VF (2011) The pstSCAB operon for phosphate uptake is regulated by the global regulator GlxR in Corynebacterium glutamicum. J Biotechnol 154:149–155

    PubMed  CAS  Article  Google Scholar 

  123. Parche S, Burkovski A, Sprenger GA, Weil B, Krämer R, Titgemeyer F (2001) Corynebacterium glutamicum: a dissection of the PTS. J Mol Microbiol Biotechnol 3:423–428

    PubMed  CAS  Google Scholar 

  124. Park SY, Moon MW, Subhadra B, Lee JK (2010) Functional characterization of the glxR deletion mutant of Corynebacterium glutamicum ATCC 13032: involvement of GlxR in acetate metabolism and carbon catabolite repression. FEMS Microbiol Lett 304:107–115

    PubMed  CAS  Article  Google Scholar 

  125. Pátek M, Nešvera J (2011) Sigma factors and promoters in Corynebacterium glutamicum. J Biotechnol 154:101–113

    PubMed  Article  CAS  Google Scholar 

  126. Pátek M, Nešvera J, Guyonvarch A, Reyes O, Leblon G (2003) Promoters of Corynebacterium glutamicum. J Biotechnol 104:311–323

    PubMed  Article  CAS  Google Scholar 

  127. Pátek M, Holátko J, Busche T, Kalinowski J, Nešvera J (2013) Corynebacterium glutamicum promoters: a practical approach. Microb Biotechnol 6:103–117

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  128. Pauling J, Röttger R, Tauch A, Azevedo V, Baumbach J (2012) CoryneRegNet 6.0—Updated database content, new analysis methods and novel features focusing on community demands. Nucleic Acids Res 40:D610–D614

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  129. Peekhaus N, Conway T (1998) Positive and negative transcriptional regulation of the Escherichia coli gluconate regulon gene gntT by GntR and the cyclic AMP (cAMP)-cAMP receptor protein complex. J Bacteriol 180:1777–1785

    PubMed  CAS  PubMed Central  Google Scholar 

  130. Peng X, Okai N, Vertès A, Inatomi K-i, Inui M, Yukawa H (2011) Characterization of the mannitol catabolic operon of Corynebacterium glutamicum. Appl Microbiol Biotechnol 91:1375–1387

    PubMed  CAS  Article  Google Scholar 

  131. Poetsch A, Haussmann U, Burkovski A (2011) Proteomics of corynebacteria: From biotechnology workhorses to pathogens. Proteomics 11:3244–3255

    PubMed  CAS  Article  Google Scholar 

  132. Polen T, Wendisch VF (2004) Genomewide expression analysis in amino acid-producing bacteria using DNA microarrays. Appl Biochem Biotechnol 118:215–232

    PubMed  CAS  Article  Google Scholar 

  133. Polen T, Schluesener D, Poetsch A, Bott M, Wendisch VF (2007) Characterization of citrate utilization in Corynebacterium glutamicum by transcriptome and proteome analysis. FEMS Microbiol Lett 273:109–119

    PubMed  CAS  Article  Google Scholar 

  134. Porco A, Peekhaus N, Bausch C, Tong S, Isturiz T, Conway T (1997) Molecular genetic characterization of the Escherichia coli gntT gene of GntI, the main system for gluconate metabolism. J Bacteriol 179:1584–1590

    PubMed  CAS  PubMed Central  Google Scholar 

  135. Reizer J, Bergstedt U, Galinier A, Küster E, Saier MH, Hillen W, Steinmetz M, Deutscher J (1996) Catabolite repression resistance of gnt operon expression in Bacillus subtilis conferred by mutation of His-15, the site of phosphoenolpyruvate-dependent phosphorylation of the phosphocarrier protein HPr. J Bacteriol 178:5480–5486

    PubMed  CAS  PubMed Central  Google Scholar 

  136. Rey DA, Nentwich SS, Koch DJ, Ruckert C, Pühler A, Tauch A, Kalinowski J (2005) The McbR repressor modulated by the effector substance S-adenosylhomocysteine controls directly the transcription of a regulon involved in sulphur metabolism of Corynebacterium glutamicum ATCC 13032. Mol Microbiol 56:871–887

    PubMed  CAS  Article  Google Scholar 

  137. Rückert C, Milse J, Albersmeier A, Koch DJ, Pühler A, Kalinowski J (2008) The dual transcriptional regulator CysR in Corynebacterium glutamicum ATCC 13032 controls a subset of genes of the McbR regulon in response to the availability of sulphide acceptor molecules. BMC Genomics 9:483

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  138. Schröder J, Tauch A (2010) Transcriptional regulation of gene expression in Corynebacterium glutamicum: the role of global, master and local regulators in the modular and hierarchical gene regulatory network. FEMS Microbiol Rev 34:685–737

    PubMed  Article  CAS  Google Scholar 

  139. Schröder J, Jochmann N, Rodionov DA, Tauch A (2010) The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 11:12

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  140. Seibold GM, Hagmann CT, Schietzel M, Emer D, Auchter M, Schreiner J, Eikmanns BJ (2010) The transcriptional regulators RamA and RamB are involved in the regulation of glycogen synthesis in Corynebacterium glutamicum. Microbiology 156:1256–1263

    PubMed  CAS  Article  Google Scholar 

  141. Shen-Orr SS, Milo R, Mangan S, Alon U (2002) Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31:64–68

    PubMed  CAS  Article  Google Scholar 

  142. Silberbach M, Burkovski A (2006) Application of global analysis techniques to Corynebacterium glutamicum: new insights into nitrogen regulation. J Biotechnol 126:101–110

    PubMed  CAS  Article  Google Scholar 

  143. Silberbach M, Huser A, Kalinowski J, Pühler A, Walter B, Kramer R, Burkovski A (2005) DNA microarray analysis of the nitrogen starvation response of Corynebacterium glutamicum. J Biotechnol 119:357–367

    PubMed  CAS  Article  Google Scholar 

  144. Subhadra B, Lee JK (2013) Elucidation of the regulation of ethanol catabolic genes and ptsG using a glxR and adenylate cyclase gene (cyaB) deletion mutants of Corynebacterium glutamicum ATCC 13032. J Microbiol Biotechnol 23:1683–1690

    PubMed  CAS  Article  Google Scholar 

  145. Subhadra B, Durga R, Han JY, Bae KH, Lee JK (2015) Identification of the regulators binding to the upstream region of glxR in Corynebacterium glutamicum. J Microbiol Biotechnol 25:1216–1226

  146. Suda M, Teramoto H, Imamiya T, Inui M, Yukawa H (2008) Transcriptional regulation of Corynebacterium glutamicum methionine biosynthesis genes in response to methionine supplementation under oxygen deprivation. Appl Microbiol Biotechnol 81:505–513

    PubMed  CAS  Article  Google Scholar 

  147. Suzuki N, Okayama S, Nonaka H, Tsuge Y, Inui M, Yukawa H (2005) Large-scale engineering of the Corynebacterium glutamicum genome. Appl Environ Microbiol 71:3369–3372

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  148. Suzuki N, Okai N, Nonaka H, Tsuge Y, Inui M, Yukawa H (2006) High-throughput transposon mutagenesis of Corynebacterium glutamicum and construction of a single-gene disruptant mutant library. Appl Environ Microbiol 72:3750–3755

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  149. Takemoto N, Tanaka Y, Inui M, Yukawa H (2014) The physiological role of riboflavin transporter and involvement of FMN-riboswitch in its gene expression in Corynebacterium glutamicum. Appl Microbiol Biotechnol 98:4159–4168

    PubMed  CAS  Article  Google Scholar 

  150. Takemoto N, Tanaka Y, Inui M (2015) Rho and RNase play a central role in FMN riboswitch regulation in Corynebacterium glutamicum. Nucleic Acids Res 43:520–529

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  151. Tanaka Y, Okai N, Teramoto H, Inui M, Yukawa H (2008a) Regulation of the expression of phosphoenolpyruvate: carbohydrate phosphotransferase system (PTS) genes in Corynebacterium glutamicum R. Microbiology 154:264–274

    PubMed  CAS  Article  Google Scholar 

  152. Tanaka Y, Teramoto H, Inui M, Yukawa H (2008b) Regulation of expression of general components of the phosphoenolpyruvate: carbohydrate phosphotransferase system (PTS) by the global regulator SugR in Corynebacterium glutamicum. Appl Microbiol Biotechnol 78:309–318

    PubMed  CAS  Article  Google Scholar 

  153. Tanaka Y, Ehira S, Teramoto H, Inui M, Yukawa H (2012) Coordinated regulation of gnd, which encodes 6-phosphogluconate dehydrogenase, by the two transcriptional regulators GntR1 and RamA in Corynebacterium glutamicum. J Bacteriol 194:6527–6536

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  154. Tanaka Y, Takemoto N, Ito T, Teramoto H, Yukawa H, Inui M (2014) Genome-wide analysis of the role of global transcriptional regulator GntR1 in Corynebacterium glutamicum. J Bacteriol 196:3249–3258

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  155. Tani TH, Khodursky A, Blumenthal RM, Brown PO, Matthews RG (2002) Adaptation to famine: a family of stationary-phase genes revealed by microarray analysis. Proc Natl Acad Sci U S A 99:13471–13476

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  156. Taniguchi H, Wendisch VF (2015) Exploring the role of sigma factor gene expression on production by Corynebacterium glutamicum: sigma factor H and FMN as example. Front Microbiol 6:740

    PubMed  PubMed Central  Article  Google Scholar 

  157. Teramoto H, Inui M, Yukawa H (2009) Regulation of expression of genes involved in quinate and shikimate utilization in Corynebacterium glutamicum. Appl Environ Microbiol 75:3461–3468

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  158. Teramoto H, Inui M, Yukawa H (2010) Regulation of genes involved in sugar uptake, glycolysis and lactate production in Corynebacterium glutamicum. Future Microbiol 5:1475–1481

    PubMed  CAS  Article  Google Scholar 

  159. Teramoto H, Inui M, Yukawa H (2011) Transcriptional regulators of multiple genes involved in carbon metabolism in Corynebacterium glutamicum. J Biotechnol 154:114–125

    PubMed  CAS  Article  Google Scholar 

  160. Townsend PD, Jungwirth B, Pojer F, Bußmann M, Money VA, Cole ST, Pühler A, Tauch A, Bott M, Cann MJ, Pohl E (2014) The crystal structures of apo and cAMP-bound GlxR from Corynebacterium glutamicum reveal structural and dynamic changes upon cAMP binding in CRP/FNR family transcription factors. PLoS One 9:e113265

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  161. Toyoda K, Teramoto H, Inui M, Yukawa H (2008) Expression of the gapA gene encoding glyceraldehyde-3-phosphate dehydrogenase of Corynebacterium glutamicum is regulated by the global regulator SugR. Appl Microbiol Biotechnol 81:291–301

    PubMed  CAS  Article  Google Scholar 

  162. Toyoda K, Teramoto H, Inui M, Yukawa H (2009a) Involvement of the LuxR-type transcriptional regulator, RamA, in regulation of expression of the gapA gene encoding glyceraldehyde-3-phosphate dehydrogenase of Corynebacterium glutamicum. J Bacteriol 191:968–977

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  163. Toyoda K, Teramoto H, Inui M, Yukawa H (2009b) The ldhA gene, encoding fermentative L-lactate dehydrogenase of Corynebacterium glutamicum, is under the control of positive feedback regulation mediated by LldR. J Bacteriol 191:4251–4258

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  164. Toyoda K, Teramoto H, Inui M, Yukawa H (2009c) Molecular mechanism of SugR-mediated sugar-dependent expression of the ldhA gene encoding L-lactate dehydrogenase in Corynebacterium glutamicum. Appl Microbiol Biotechnol 83:315–327

    PubMed  CAS  Article  Google Scholar 

  165. Toyoda K, Teramoto H, Inui M, Yukawa H (2011) Genome-wide identification of in vivo binding sites of GlxR, a cyclic AMP receptor protein-type regulator in Corynebacterium glutamicum. J Bacteriol 193:4123–4133

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  166. Toyoda K, Teramoto H, Gunji W, Inui M, Yukawa H (2013) Involvement of regulatory interactions among global regulators GlxR, SugR, and RamA in expression of ramA in Corynebacterium glutamicum. J Bacteriol 195:1718–1726

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  167. Toyoda K, Teramoto H, Yukawa H, Inui M (2015) Expanding the regulatory network governed by the extracytoplasmic function sigma factor σH in Corynebacterium glutamicum. J Bacteriol 197:483–496

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  168. Trötschel C, Albaum SP, Poetsch A (2013) Proteome turnover in bacteria: current status for Corynebacterium glutamicum and related bacteria. Microb Biotechnol 6:708–719

    PubMed  PubMed Central  Google Scholar 

  169. Tryfona T, Bustard MT (2006) Enhancement of biomolecule transport by electroporation: a review of theory and practical application to transformation of Corynebacterium glutamicum. Biotechnol Bioeng 93:413–423

    PubMed  CAS  Article  Google Scholar 

  170. van Ooyen J, Emer D, Bussmann M, Bott M, Eikmanns BJ, Eggeling L (2011) Citrate synthase in Corynebacterium glutamicum is encoded by two gltA transcripts which are controlled by RamA, RamB, and GlxR. J Biotechnol 154:140–148

    PubMed  Article  CAS  Google Scholar 

  171. Vertès AA, Inui M, Yukawa H (2005) Manipulating corynebacteria, from individual genes to chromosomes. Appl Environ Microbiol 71:7633–7642

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  172. Vertès AA, Inui M, Yukawa H (2012) Postgenomic approaches to using corynebacteria as biocatalysts. Annu Rev Microbiol 66:521–550

    PubMed  Article  CAS  Google Scholar 

  173. Wade JT, Struhl K, Busby SJ, Grainger DC (2007) Genomic analysis of protein-DNA interactions in bacteria: insights into transcription and chromosome organization. Mol Microbiol 65:21–26

    PubMed  CAS  Article  Google Scholar 

  174. Wendisch VF (2014) Microbial production of amino acids and derived chemicals: synthetic biology approaches to strain development. Curr Opin Biotechnol 30:51–58

    PubMed  CAS  Article  Google Scholar 

  175. Wendisch VF, de Graaf AA, Sahm H, Eikmanns BJ (2000) 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 182:3088–3096

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  176. Wendisch VF, Bott M, Kalinowski J, Oldiges M, Wiechert W (2006) Emerging Corynebacterium glutamicum systems biology. J Biotechnol 124:74–92

    PubMed  CAS  Article  Google Scholar 

  177. Wennerhold J, Bott M (2006) The DtxR regulon of Corynebacterium glutamicum. J Bacteriol 188:2907–2918

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  178. Wennerhold J, Krug A, Bott M (2005) 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 280:40500–40508

    PubMed  CAS  Article  Google Scholar 

  179. Wieschalka S, Blombach B, Bott M, Eikmanns BJ (2013) Bio-based production of organic acids with Corynebacterium glutamicum. Microb Biotechnol 6:87–102

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  180. Woo HM, Park J-B (2014) Recent progress in development of synthetic biology platforms and metabolic engineering of Corynebacterium glutamicum. J Biotechnol 180:43–51

    PubMed  CAS  Article  Google Scholar 

  181. Young IG, Jaworowski A, Poulis M (1982) Cloning of the gene for the respiratory D-lactate dehydrogenase of Escherichia coli. Biochemistry 21:2092–2095

    PubMed  CAS  Article  Google Scholar 

  182. Yukawa H, Omumasaba CA, Nonaka H, Kós P, Okai N, Suzuki N, Suda M, Tsuge Y, Watanabe J, Ikeda Y, Vertès AA, Inui M (2007) Comparative analysis of the Corynebacterium glutamicum group and complete genome sequence of strain R. Microbiology 153:1042–1058

    PubMed  CAS  Article  Google Scholar 

  183. Zemanová M, Kaderábková P, Pátek M, Knoppová M, Silar R, Nesvera J (2008) Chromosomally encoded small antisense RNA in Corynebacterium glutamicum. FEMS Microbiol Lett 279:195–201

    PubMed  Article  CAS  Google Scholar 

  184. Zheng D, Constantinidou C, Hobman JL, Minchin SD (2004) Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32:5874–5893

    PubMed  CAS  PubMed Central  Article  Google Scholar 

Download references

Author information

Affiliations

  1. Research institute of Innovative Technology for the Earth (RITE), 9-2 Kizugawadai, Kizugawa, Kyoto, Japan

    Koichi Toyoda & Masayuki Inui

  2. Graduate School of Biological Sciences, Nara Institute of Science and Technology, Nara, Japan

    Masayuki Inui

Authors
  1. Koichi Toyoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayuki Inui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masayuki Inui.

Ethics declarations

Conflict of interest

Koichi Toyoda declares that he has no conflict of interest. Masayuki Inui declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Toyoda, K., Inui, M. Regulons of global transcription factors in Corynebacterium glutamicum . Appl Microbiol Biotechnol 100, 45–60 (2016). https://doi.org/10.1007/s00253-015-7074-3

Download citation

Keywords

  • Corynebacterium glutamicum
  • Transcriptional regulatory network
  • Chromatin immunoprecipitation
  • Transcriptional regulation
  • Transcription factor
  • Regulon