Identification of the cAMP phosphodiesterase CpdA as novel key player in cAMP-dependent regulation in Corynebacterium glutamicum

Molecular Microbiology

Volumn 103, Issue 3, 2017, Pages 534-552

  Schulte, Julia ^a   Baumgart, Meike ^a   Bott, Michael ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP PHOSPHODIESTERASE; GLUCOSE; MESSENGER RNA; PROTEIN CPDA; PROTEIN GLXR; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; PROTEIN BINDING;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM MUTANT; CARBON SOURCE; CELL LEVEL; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; ENZYME ANALYSIS; ENZYME PURIFICATION; GROWTH RATE; NEGATIVE FEEDBACK; NONHUMAN; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

3',5'-CYCLIC-AMP PHOSPHODIESTERASES; BACTERIAL PROTEINS; CORYNEBACTERIUM GLUTAMICUM; CYCLIC AMP; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN BINDING;

EID: 85008255923     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13574     Document Type: Article

References (90)

1. Arndt, A., and Eikmanns, B.J. (2007) The alcohol dehydrogenase gene adhA in Corynebacterium glutamicum is subject to carbon catabolite repression. J Bacteriol 189: 7408–7416.
2. Arndt, A., Auchter, M., Ishige, T., Wendisch, V.F., and Eikmanns, B.J. (2008) Ethanol catabolism in Corynebacterium glutamicum. J Mol Microbiol Biotechnol 15: 222–233.
3. Auchter, M., Arndt, A., and Eikmanns, B.J. (2009) Dual transcriptional control of the acetaldehyde dehydrogenase gene ald of Corynebacterium glutamicum by RamA and RamB. J Biotechnol 140: 84–91.
4. Baumgart, M., and Bott, M. (2011) Biochemical characterisation of aconitase from Corynebacterium glutamicum. J Biotechnol 154: 163–170.
5. Baumgart, M., Luder, K., Grover, S., Gätgens, C., Besra, G.S., and Frunzke, J. (2013) IpsA, a novel LacI-type regulator, is required for inositol-derived lipid formation in Corynebacteria and Mycobacteria. BMC Biol 11: 122.
6. Becker, J., and Wittmann, C. (2012) Bio-based production of chemicals, materials and fuels -Corynebacterium glutamicum as versatile cell factory. Curr Opin Biotechnol 23: 631–640.
7. Boratyn, G.M., Schaffer, A.A., Agarwala, R., Altschul, S.F., Lipman, D.J., and Madden, T.L. (2012) Domain enhanced lookup time accelerated BLAST. Biol Direct 7: 12.
8. Botsford, J.L., and Harman, J.G. (1992) Cyclic AMP in prokaryotes. Microbiol Rev 56: 100–122.
9. Bott, M. (2007) Offering surprises: TCA cycle regulation in Corynebacterium glutamicum. Trends Microbiol 15: 417–425.
10. Brocker, M., Schaffer, S., Mack, C., and 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.
11. Burkovski, A. (ed) (2008) Corynebacteria: Genomics and Molecular biology. Norfolk, UK: Caister Academic Press.
12. Burkovski, A. (ed) (2015) Corynebacterium glutamicum - From Systems Biology to Biotechnological Applications. Norfolk, UK: Caister Academic Press.
13. Busby, S., and Ebright, R.H. (1999) Transcription activation by catabolite activator protein (CAP). J Mol Biol 293: 199–213.
14. Bussmann, M., Baumgart, M., and Bott, M. (2010) RosR (Cg1324), a hydrogen peroxide-sensitive MarR-type transcriptional regulator of Corynebacterium glutamicum. J Biol Chem 285: 29305–29318.
15. Bussmann, M., Emer, D., Hasenbein, S., Degraf, S., Eikmanns, B.J., and 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.
16. Callahan, S.M., Cornell, N.W., and Dunlap, P.V. (1995) Purification and properties of periplasmic 3':5'-cyclic nucleotide phosphodiesterase. A novel zinc-containing enzyme from the marine symbiotic bacterium Vibrio fischeri. J Biol Chem 270: 17627–17632.
17. Cha, P.H., Park, S.Y., Moon, M.W., Subhadra, B., Oh, T.K., Kim, E., et al. (2010) Characterization of an adenylate cyclase gene (cyaB) deletion mutant of Corynebacterium glutamicum ATCC 13032. Appl Microbiol Biotechnol 85: 1061–1068.
18. Conti, M., and Beavo, J. (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481–511.
19. Cramer, A., Gerstmeir, R., Schaffer, S., Bott, M., and Eikmanns, B.J. (2006) Identification of RamA, a novel LuxR-type transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol 188: 2554–2567.
20. Cremer, J., Eggeling, L., and Sahm, H. (1990) Cloning the dapA dapB cluster of the lysine-secreting bacterium Corynebacterium glutamicum. Mol Gen Genet 220: 478–480.
21. Dunlap, P.V., and Callahan, S.M. (1993) Characterization of a periplasmic 3':5'-cyclic nucleotide phosphodiesterase gene, cpdP, from the marine symbiotic bacterium Vibrio fischeri. J Bacteriol 175: 4615–4624.
22. Eggeling, L., and Bott, M. (eds) (2005) Handbook of Corynebacterium glutamicum. Boca Raton, FL: CRC Press, Taylor & Francis Group.
23. Eggeling, L., and Bott, M. (2015) A giant market and a powerful metabolism: L-lysine provided by Corynebacterium glutamicum. Appl Microbiol Biotechnol 99: 3387–3394.
24. Eikmanns, B.J., Kleinertz, E., Liebl, W., and Sahm, H. (1991) A family of Corynebacterium glutamicum/Escherichia coli shuttle vectors for cloning, controlled gene expression, and promoter probing. Gene 102: 93–98.
25. Engels, V., and Wendisch, V.F. (2007) The DeoR-type regulator SugR represses expression of ptsG in Corynebacterium glutamicum. J Bacteriol 189: 2955–2966.
26. Fernley, H.N., and Walker, P.G. (1967) Studies on alkaline phosphatase. Inhibition by phosphate derivatives and the substrate specificity. Biochem J 104: 1011–1018.
27. Frunzke, J., Engels, V., Hasenbein, S., Gätgens, C., and 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.
28. Fuchs, E.L., Brutinel, E.D., Klem, E.R., Fehr, A.R., Yahr, T.L., and Wolfgang, M.C. (2010) In vitro and in vivo characterization of the Pseudomonas aeruginosa cyclic AMP (cAMP) phosphodiesterase CpdA, required for cAMP homeostasis and virulence factor regulation. J Bacteriol 192: 2779–2790.
29. Gerstmeir, R., Cramer, A., Dangel, P., Schaffer, S., and Eikmanns, B.J. (2004) RamB, a novel transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol 186: 2798–2809.
30. Gibson, D.G., Young, L., Chuang, R.Y., Venter, J.C., Hutchison, C.A., and Smith, H.O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Meth 6: 343–345.
31. Gomelsky, M. (2011) cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol Microbiol 79: 562–565.
32. Görke, B., and Stülke, J. (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6: 613–624.
33. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557–580.
34. Hantke, K., Winkler, K., and Schultz, J.E. (2011) Escherichia coli exports cyclic AMP via TolC. J Bacteriol 193: 1086–1089.
35. Hermann, T. (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104: 155–172.
36. Hong, E.J., Park, J.S., Kim, Y., and Lee, H.S. (2014) Role of Corynebacterium glutamicum sprA encoding a serine protease in glxR-mediated global gene regulation. PLoS One 9: e93587.
37. Hoyer, L.L., Cieslinski, L.B., McLaughlin, M.M., Torphy, T.J., Shatzman, A.R., and Livi, G.P. (1994) A Candida albicans cyclic nucleotide phosphodiesterase: cloning and expression in Saccharomyces cerevisiae and biochemical characterization of the recombinant enzyme. Microbiology 140: 1533–1542.
38. Imamura, R., Yamanaka, K., Ogura, T., Hiraga, S., Fujita, N., Ishihama, A., and Niki, H. (1996) Identification of the cpdA gene encoding cyclic 3′,5′-adenosine monophosphate phosphodiesterase in Escherichia coli. J Biol Chem 271: 25423–25429.
39. Ingram, L.O. (1990) Ethanol tolerance in bacteria. Crit Rev Biotechnol 9: 305–319.
40. Jakoby, M., Ngouoto-Nkili, C.E., and Burkovski, A. (1999) Construction and application of new Corynebacterium glutamicum vectors. Biotechnol Techniq 13: 437–441.
41. Jungwirth, B., Emer, D., Brune, I., Hansmeier, N., Pühler, A., Eikmanns, B.J., and 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.
42. Jungwirth, B., Sala, C., Kohl, T.A., Uplekar, S., Baumbach, J., Cole, S.T., et al. (2013) High-resolution detection of DNA binding sites of the global transcriptional regulator GlxR in Corynebacterium glutamicum. Microbiology 159: 12–22.
43. Kalivoda, E.J., Brothers, K.M., Stella, N.A., Schmitt, M.J., and Shanks, R.M. (2013) Bacterial cyclic AMP-phosphodiesterase activity coordinates biofilm formation. PLoS One 8: e71267.
44. Kim, H.J., Kim, T.H., Kim, Y., and Lee, H.S. (2004) Identification and characterization of glxR, a gene involved in regulation of glyoxylate bypass in Corynebacterium glutamicum. J Bacteriol 186: 3453–3460.
45. Kim, H.S., Kim, S.M., Lee, H.J., Park, S.J., and Lee, K.H. (2009) Expression of the cpdA gene, encoding a 3′,5′-cyclic AMP (cAMP) phosphodiesterase, is positively regulated by the cAMP-cAMP receptor protein complex. J Bacteriol 191: 922–930.
46. Kimura, Y., Okazaki, N., and Takegawa, K. (2009) Enzymatic characteristics of two novel Myxococcus xanthus enzymes, PdeA and PdeB, displaying 3′,5′- and 2′,3′-cAMP phosphodiesterase, and phosphatase activities. FEBS Lett 583: 443–448.
47. Kimura, Y., Yoshimi, M., and Takata, G. (2011) Enzymatic and mutational analyses of a class II 3′,5′-cyclic nucleotide phosphodiesterase, PdeE, from Myxococcus xanthus. J Bacteriol 193: 2053–2057.
48. Kimura, Y., Nakatuma, H., Sato, N., and Ohtani, M. (2006) Contribution of the cyclic nucleotide phosphodiesterases PdeA and PdeB to adaptation of Myxococcus xanthus cells to osmotic or high-temperature stress. J Bacteriol 188: 823–828.
49. Kinoshita, S., Udaka, S., and Shimono, M. (1957) Studies on amino acid fermentation. Part I. Production of L-glutamic acid by various microorganisms. J Gen Appl Microbiol 3: 193–205.
50. Kohl, T.A., and 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.
51. Kohl, T.A., Baumbach, J., Jungwirth, B., Pühler, A., and 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.
52. Kolb, A., Busby, S., Buc, H., Garges, S., and Adhya, S. (1993) Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62: 749–795.
53. Kortmann, M., Kuhl, V., Klaffl, S., and Bott, M. (2015) A chromosomally encoded T7 RNA polymerase-dependent gene expression system for Corynebacterium glutamicum: construction and comparative evaluation at the single-cell level. Microb Biotechnol 8: 253–265.
54. Krämer, R., Lambert, C., Hoischen, C., and Ebbighausen, H. (1990) Uptake of glutamate in Corynebacterium glutamicum. 1. Kinetic properties and regulation by internal pH and potassium. Eur J Biochem 194: 929–935.
55. Lacombe, M.L., Podgorski, G.J., Franke, J., and Kessin, R.H. (1986) Molecular cloning and developmental expression of the cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum. J Biol Chem 261: 16811–16817.
56. Letek, M., Valbuena, N., Ramos, A., Ordóñez, E., Gil, J.A., and Mateos, L.M. (2006) Characterization and use of catabolite-repressed promoters from gluconate genes in Corynebacterium glutamicum. J Bacteriol 188: 409–423.
57. m cyclic nucleotide phosphodiesterase of bakers' yeast. J Biol Chem 258: 2966–2972.
58. Ma, P., Wera, S., Van Dijck, P., and Thevelein, J.M. (1999) The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell 10: 91–104.
59. Malan, T.P., Kolb, A., Buc, H., and McClure, W.R. (1984) Mechanism of CRP-cAMP activation of lac operon transcription initiation activation of the P1 promoter. J Mol Biol 180: 881–909.
60. Marden, J.N., Dong, Q., Roychowdhury, S., Berleman, J.E., and Bauer, C.E. (2011) Cyclic GMP controls Rhodospirillum centenum cyst development. Mol Microbiol 79: 600–615.
61. 1. Arch Microbiol 175: 282–294.
62. Ochoa De Alda, J.A., Ajlani, G., and Houmard, J. (2000) Synechocystis strain PCC 6803 cya2, a prokaryotic gene that encodes a guanylyl cyclase. J Bacteriol 182: 3839–3842.
63. Park, S.Y., Moon, M.W., Subhadra, B., and Lee, J.K. (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.
64. Pauling, J., Röttger, R., Tauch, A., Azevedo, V., and 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.
65. Pfeifer-Sancar, K., Mentz, A., Rückert, C., and Kalinowski, J. (2013) Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique. BMC Genomics 14: 888.
66. Polen, T., Schluesener, D., Poetsch, A., Bott, M., and Wendisch, V.F. (2007) Characterization of citrate utilization in Corynebacterium glutamicum by transcriptome and proteome analysis. FEMS Microbiol Lett 273: 109–119.
67. Rauch, A., Leipelt, M., Russwurm, M., and Steegborn, C. (2008) Crystal structure of the guanylyl cyclase Cya2. Proc Natl Acad Sci USA 105: 15720–15725.
68. Reinscheid, D.J., Schnicke, S., Rittmann, D., Zahnow, U., Sahm, H., and Eikmanns, B.J. (1999) Cloning, sequence analysis, expression and inactivation of the Corynebacterium glutamicum pta-ack operon encoding phosphotransacetylase and acetate kinase. Microbiology 145: 503–513.
69. Richter, W. (2002) 3′,5′ Cyclic nucleotide phosphodiesterases class III: members, structure, and catalytic mechanism. Proteins 46: 278–286.
70. Sambrook, J., and Russell, D. (2001) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
71. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G., and Pühler, A. (1994) Small mobilizable multipurpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19 - Selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69–73.
72. Schröder, J., and 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.
73. Shenoy, A.R., Sreenath, N., Podobnik, M., Kovačevič, M., and Visweswariah, S.S. (2005) The Rv0805 gene from Mycobacterium tuberculosis encodes a 3′,5′-cyclic nucleotide phosphodiesterase: biochemical and mutational analysis. Biochemistry 44: 15695–15704.
74. Shenoy, A.R., Capuder, M., Draškovič, P., Lamba, D., Visweswariah, S.S., and Podobnik, M. (2007) Structural and biochemical analysis of the Rv0805 cyclic nucleotide phosphodiesterase from Mycobacterium tuberculosis. J Mol Biol 365: 211–225.
75. Shuman, H.A., and Silhavy, T.J. (2003) The art and design of genetic screens: Escherichia coli. Nat Rev Genet 4: 419–431.
76. Sismeiro, O., Trotot, P., Biville, F., Vivares, C., and Danchin, A. (1998) Aeromonas hydrophila adenylyl cyclase 2: a new class of adenylyl cyclases with thermophilic properties and sequence similarities to proteins from hyperthermophilic archaebacteria. J Bacteriol 180: 3339–3344.
77. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76–85.
78. Subhadra, B., and Lee, J.K. (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.
79. Subhadra, B., Ray, D., Han, J.Y., Bae, K.H., and Lee, J.K. (2015) Identification of the regulators binding to the upstream region of glxR in Corynebacterium glutamicum. J Microbiol Biotechnol 25: 1216–1226.
80. Tagami, H., and Aiba, H. (1998) A common role of CRP in transcription activation: CRP acts transiently to stimulate events leading to open complex formation at a diverse set of promoters. EMBO J 17: 1759–1767.
81. Tauch, A., Kirchner, O., Löffler, B., Gotker, S., Pühler, A., and Kalinowski, J. (2002) Efficient electrotransformation of Corynebacterium diphtheriae with a mini-replicon derived from the Corynebacterium glutamicum plasmid pGA1. Curr Microbiol 45: 362–367.
82. Tian, Y., Cui, W., Huang, M., Robinson, H., Wan, Y., Wang, Y., and Ke, H. (2014) Dual specificity and novel structural folding of yeast phosphodiesterase-1 for hydrolysis of second messengers cyclic adenosine and guanosine 3',5'-monophosphate. Biochemistry 53: 4938–4945.
83. Townsend, P.D., Jungwirth, B., Pojer, F., Bussmann, M., Money, V.A., Cole, S.T., et al. (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.
84. Toyoda, K., and Inui, M. (2016) Regulons of global transcription factors in Corynebacterium glutamicum. Appl Microbiol Biotechnol 100: 45–60.
85. Toyoda, K., Teramoto, H., Inui, M., and Yukawa, H. (2009) 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.
86. Toyoda, K., Teramoto, H., Inui, M., and 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.
87. Vogt, M., Haas, S., Klaffl, S., Polen, T., Eggeling, L., van Ooyen, J., and Bott, M. (2014) Pushing product formation to its limit: metabolic engineering of Corynebacterium glutamicum for L-leucine overproduction. Metab Eng 22: 40–52.
88. Wendisch, V.F., Jorge, J.M., Perez-Garcia, F., and Sgobba, E. (2016) Updates on industrial production of amino acids using Corynebacterium glutamicum. World J Microbiol Biotechnol 32: 105.
89. Yukawa, H., and Inui, M. (eds) (2013) Corynebacterium glutamicum: Biology and Biotechnology. Heidelberg: Springer.
90. Zheng, Z., Zhu, M., He, Y., Li, N., Guo, T., Chen, Y., et al. (2013) Gene cloning, expression, and characterization of a cyclic nucleotide phosphodiesterase from Arthrobacter sp. CGMCC 3584. Appl Biochem Biotechnol 169: 2442–2456.