Three genes encoding citrate synthases in saccharopolyspora erythraea are regulated by the global nutrient-sensing regulators glnr, dasr, and crp

Molecular Microbiology

Volumn 94, Issue 5, 2014, Pages 1065-1084

  Liao, Cheng Heng ^a   Yao, Li li ^a   Ye, Bang Ce ^a  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOSUGAR; CARBON; CHITIN; CITRATE SYNTHASE; CYCLIC AMP; NITROGEN; PROTEIN CRP; PROTEIN DASR; PROTEIN GLNR; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BINDING COMPETITION; CARBOHYDRATE METABOLISM; CARBON METABOLISM; CELL LEVEL; CITA GENE; CITA4 GENE; CONTROLLED STUDY; DNA FOOTPRINTING; ENZYME ANALYSIS; ENZYME REGULATION; GEL MOBILITY SHIFT ASSAY; GENETIC REGULATION; GLTA 2 GENE; NITROGEN METABOLISM; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; SACCHAROPOLYSPORA; SACCHAROPOLYSPORA ERYTHRAEA; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION;

SACCHAROPOLYSPORA ERYTHRAEA;

EID: 84912047242     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12818     Document Type: Article

References (70)

1. Amon, J., Titgemeyer, F., and Burkovski, A. (2010) Common patterns - unique features: nitrogen metabolism and regulation in Gram-positive bacteria. FEMS Microbiol Rev 34: 588-605.
2. Busby, S., and Ebright, R.H. (1997) Transcription activation at class II CAP-dependent promoters. Mol Microbiol 23: 853-859.
3. Carata, E., Peano, C., Tredici, S.M., Ferrari, F., Tala, A., Corti, G., etal. (2009) Phenotypes and gene expression profiles of Saccharopolyspora erythraea rifampicin-resistant (rif) mutants affected in erythromycin production. Microb Cell Fact 8: 18.
4. Cheung, J., Murphy, M.E., and Heinrichs, D.E. (2012) Discovery of an iron-regulated citrate synthase in Staphylococcus aureus. Chem Biol 19: 1568-1578.
5. Claes, W.A., Pühler, A., and Kalinowski, J. (2002) Identification of two prpDBC gene clusters in Corynebacterium glutamicum and their involvement in propionate degradation via the 2-methylcitrate cycle. J Bacteriol 184: 2728-2739.
6. Colson, S., Stephan, J., Hertrich, T., Saito, A., van Wezel, G.P., Titgemeyer, F., and Rigali, S. (2007) Conserved cis-acting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J Mol Microbiol Biotechnol 12: 60-66.
7. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., etal. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
8. Derouaux, A., Dehareng, D., Lecocq, E., Halici, S., Nothaft, H., Giannotta, F., etal. (2004a) Crp of Streptomyces coelicolor is the third transcription factor of the large CRP-FNR superfamily able to bind cAMP. Biochem Biophys Res Commun 325: 983-990.
9. Derouaux, A., Halici, S., Nothaft, H., Neutelings, T., Moutzourelis, G., Dusart, J., etal. (2004b) Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J Bacteriol 186: 1893-1897.
10. Dingman, D.W., Rosenkrantz, M.S., and Sonenshein, A.L. (1987) Relationship between aconitase gene expression and sporulation in Bacillus subtilis. J Bacteriol 169: 3068-3075.
11. Donald, L.J., Molgat, G.F., and Duckworth, H.W. (1989) Cloning, sequencing, and expression of the gene for NADH-sensitive citrate synthase of Pseudomonas aeruginosa. J Bacteriol 171: 5542-5550.
12. Eidels, L., and Preiss, J. (1970) Citrate synthase. A regulatory enzyme from Rhodopseudomonas capsulata. J Biol Chem 245: 2937-2945.
13. Eikmanns, B.J., Thum-Schmitz, N., Eggeling, L., Ludtke, K.U., and Sahm, H. (1994) Nucleotide sequence, expression and transcriptional analysis of the Corynebacterium glutamicum gltA gene encoding citrate synthase. Microbiology 140 (Part 8): 1817-1828.
14. Emmer, M., deCrombrugghe, B., Pastan, I., and Perlman, R. (1970) Cyclic AMP receptor protein of E. coli: its role in the synthesis of inducible enzymes. Proc Natl Acad Sci USA 66: 480-487.
15. Fic, E., Bonarek, P., Gorecki, A., Kedracka-Krok, S., Mikolajczak, J., Polit, A., etal. (2009) cAMP receptor protein from Escherichia coli as a model of signal transduction in proteins - a review. J Mol Microbiol Biotechnol 17: 1-11.
16. Fink, D., Weissschuh, N., Reuther, J., Wohlleben, W., and Engels, A. (2002) Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 46: 331-347.
17. Flechtner, V.R., and Hanson, R.S. (1969) Coarse and fine control of citrate synthase from Bacillus subtilis. Biochim Biophys Acta 184: 252-262.
18. Francois, J.A., Starks, C.M., Sivanuntakorn, S., Jiang, H., Ransome, A.E., Nam, J.W., etal. (2006) Structure of a NADH-insensitive hexameric citrate synthase that resists acid inactivation. Biochemistry 45: 13487-13499.
19. Fujita, Y. (2009) Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci Biotechnol Biochem 73: 245-259.
20. Gao, C., Hindra, Mulder, D., Yin, C., and Elliot, M.A. (2012) Crp is a global regulator of antibiotic production in streptomyces. MBio 3: pii: e00407-12.
21. Gerike, U., Hough, D.W., Russell, N.J., Dyall-Smith, M.L., and Danson, M.J. (1998) Citrate synthase and 2-methylcitrate synthase: structural, functional and evolutionary relationships. Microbiology 144 (Part 4): 929-935.
22. Gosset, G., Zhang, Z., Nayyar, S., Cuevas, W.A., and Saier, M.H., Jr (2004) Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli. J Bacteriol 186: 3516-3524.
23. Guest, J.R. (1981) Hybrid plasmids containing the citrate synthase gene (gltA) of Escherichia coli K12. J Gen Microbiol 124: 17-23.
24. Han, S., Song, P., Ren, T., Huang, X., Cao, C., and Zhang, B. (2011) Identification of SACE_7040, a member of TetR family related to the morphological differentiation of Saccharopolyspora erythraea. Curr Microbiol 63: 121-125.
25. Harford, S., and Weitzman, P.D. (1975) Evidence of isosteric and allosteric nucleotide inhibition of citrate synthease from multiple-inhibition studies. Biochem J 151: 455-458.
26. Hopwood, D.A., Bibb, M.J., Chater, K.F., Kieser, T., Bruton, C.J., and Kieser, H. (1985) Genetic Manipulation of Streptomyces: A Laboratory Manual. Norwich: The John Innes Foundation.
27. Iuchi, S., and Lin, E.C. (1988) arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc Natl Acad Sci USA 85: 1888-1892.
28. Jia, Y.K., Becam, A.M., and Herbert, C.J. (1997) The CIT3 gene of Saccharomyces cerevisiae encodes a second mitochondrial isoform of citrate synthase. Mol Microbiol 24: 53-59.
29. Jin, S., and Sonenshein, A.L. (1994a) Identification of two distinct Bacillus subtilis citrate synthase genes. J Bacteriol 176: 4669-4679.
30. Jin, S., and Sonenshein, A.L. (1994b) Transcriptional regulation of Bacillus subtilis citrate synthase genes. J Bacteriol 176: 4680-4690.
31. Jin, S., and Sonenshein, A.L. (1996) Characterization of the major citrate synthase of Bacillus subtilis. J Bacteriol 178: 3658-3660.
32. Jourlin-Castelli, C., Mani, N., Nakano, M.M., and Sonenshein, A.L. (2000) CcpC, a novel regulator of the LysR family required for glucose repression of the citB gene in Bacillus subtilis. J Mol Biol 295: 865-878.
33. Khankal, R., Chin, J.W., Ghosh, D., and Cirino, P.C. (2009) Transcriptional effects of CRP* expression in Escherichia coli. J Biol Eng 3: 13.
34. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich: John Innes Foundation.
35. Kim, H.J., Roux, A., and Sonenshein, A.L. (2002) Direct and indirect roles of CcpA in regulation of Bacillus subtilis Krebs cycle genes. Mol Microbiol 45: 179-190.
36. Kim, K.S., Rosenkrantz, M.S., and Guarente, L. (1986) Saccharomyces cerevisiae contains two functional citrate synthase genes. Mol Cell Biol 6: 1936-1942.
37. 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.
38. 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.
39. Liao, C., Rigali, S., Cassani, C.L., Saldana, E.M., Nielsen, L.K., and Ye, B.C. (2014) Control of chitin and N-acetylglucosamine utilization in Saccharopolyspora erythraea. Microbiology 160: 1914-1928.
40. Min, I.S., Bang, J.Y., Seo, S.W., Lee, C.H., and Maeng, P.J. (2010) Differential expression of citA gene encoding the mitochondrial citrate synthase of Aspergillus nidulans in response to developmental status and carbon sources. J Microbiol 48: 188-198.
41. Mittal, M., Picossi, S., and Sonenshein, A.L. (2009) CcpC-dependent regulation of citrate synthase gene expression in Listeria monocytogenes. J Bacteriol 191: 862-872.
42. Nguyen, N.T., Maurus, R., Stokell, D.J., Ayed, A., Duckworth, H.W., and Brayer, G.D. (2001) Comparative analysis of folding and substrate binding sites between regulated hexameric type II citrate synthases and unregulated dimeric type I enzymes. Biochemistry 40: 13177-13187.
43. Nishimura, T., Teramoto, H., Toyoda, K., Inui, M., and Yukawa, H. (2011) Regulation of the nitrate reductase operon narKGHJI by the cAMP-dependent regulator GlxR in Corynebacterium glutamicum. Microbiology 157: 21-28.
44. van Ooyen, J., Emer, D., Bussmann, M., Bott, M., Eikmanns, B.J., and 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.
45. van Ooyen, J., Noack, S., Bott, M., Reth, A., and Eggeling, L. (2012) Improved L-lysine production with Corynebacterium glutamicum and systemic insight into citrate synthase flux and activity. Biotechnol Bioeng 109: 2070-2081.
46. Park, S.J., McCabe, J., Turna, J., and Gunsalus, R.P. (1994) Regulation of the citrate synthase (gltA) gene of Escherichia coli in response to anaerobiosis and carbon supply: role of the arcA gene product. J Bacteriol 176: 5086-5092.
47. Piette, A., Derouaux, A., Gerkens, P., Noens, E.E., Mazzucchelli, G., Vion, S., etal. (2005) From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J Proteome Res 4: 1699-1708.
48. Pullan, S.T., Chandra, G., Bibb, M.J., and Merrick, M. (2011) Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes. BMC Genomics 12: 175.
49. Remington, S.J. (1992) Structure and mechanism of citrate synthase. Curr Top Cell Regul 33: 209-229.
50. Rigali, S., Schlicht, M., Hoskisson, P., Nothaft, H., Merzbacher, M., Joris, B., and Titgemeyer, F. (2004) Extending the classification of bacterial transcription factors beyond the helix-turn-helix motif as an alternative approach to discover new cis/trans relationships. Nucleic Acids Res 32: 3418-3426.
51. Rigali, S., Nothaft, H., Noens, E.E., Schlicht, M., Colson, S., Müller, M., etal. (2006) The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol Microbiol 61: 1237-1251.
52. Rigali, S., Titgemeyer, F., Barends, S., Mulder, S., Thomae, A.W., Hopwood, D.A., and van Wezel, G.P. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675.
53. Santos-Beneit, F., Rodríguez-García, A., Sola-Landa, A., and Martín, J.F. (2009) Cross-talk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol Microbiol 72: 53-68.
54. Shimada, T., Fujita, N., Yamamoto, K., and Ishihama, A. (2011) Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS ONE 6: e20081.
55. Sola-Landa, A., Rodríguez-García, A., Amin, R., Wohlleben, W., and Martín, J.F. (2013) Competition between the GlnR and PhoP regulators for the glnA and amtB promoters in Streptomyces coelicolor. Nucleic Acids Res 41: 1767-1782.
56. Sonenshein, A.L. (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917-927.
57. Suissa, M., Suda, K., and Schatz, G. (1984) Isolation of the nuclear yeast genes for citrate synthase and fifteen other mitochondrial proteins by a new screening method. EMBO J 3: 1773-1781.
58. Teramoto, H., Inui, M., and Yukawa, H. (2011) Transcriptional regulators of multiple genes involved in carbon metabolism in Corynebacterium glutamicum. J Biotechnol 154: 114-125.
59. Tiffert, Y., Supra, P., Wurm, R., Wohlleben, W., Wagner, R., and Reuther, J. (2008) The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 67: 861-880.
60. Viollier, P.H., Minas, W., Dale, G.E., Folcher, M., and Thompson, C.J. (2001) Role of acid metabolism in Streptomyces coelicolor morphological differentiation and antibiotic biosynthesis. J Bacteriol 183: 3184-3192.
61. Wang, Y., Cen, X.F., Zhao, G.P., and Wang, J. (2012) Characterization of a new GlnR binding box in the promoter of amtB in Streptomyces coelicolor inferred a PhoP/GlnR competitive binding mechanism for transcriptional regulation of amtB. J Bacteriol 194: 5237-5244.
62. Weitzman, P.D. (1966) Regulation of citrate synthase activity in Escherichia coli. Biochim Biophys Acta 128: 213-215.
63. Weitzman, P.D., and Danson, M.J. (1976) Citrate synthase. Curr Top Cell Regul 10: 161-204.
64. Weitzman, P.D., and Dunmore, P. (1969a) Citrate synthases: allosteric regulation and molecular size. Biochim Biophys Acta 171: 198-200.
65. Weitzman, P.D., and Dunmore, P. (1969b) Regulation of citrate synthase activity by alpha-ketoglutarate. Metabolic and taxonomic significance. FEBS Lett 3: 265-267.
66. Weitzman, P.D., and Jones, D. (1968) Regulation of citrate synthase and microbial taxonomy. Nature 219: 270-272.
67. Wilde, R.J., and Guest, J.R. (1986) Transcript analysis of the citrate synthase and succinate dehydrogenase genes of Escherichia coli K12. J Gen Microbiol 132: 3239-3251.
68. Wilkinson, C.J., Hughes-Thomas, Z.A., Martin, C.J., Böhm, I., Mironenko, T., Deacon, M., etal. (2002) Increasing the efficiency of heterologous promoters in actinomycetes. J Mol Microbiol Biotechnol 4: 417-426.
69. Wright, J.A., Maeba, P., and Sanwal, B.D. (1967) Allosteric regulation of the activity of citrate synthetase of Escherichia coli by alpha-ketoglutarate. Biochem Biophys Res Commun 29: 34-38.
70. Yao, L.L., Liao, C.H., Huang, G., Zhou, Y., Rigali, S., Zhang, B., and Ye, B.C. (2014) GlnR-mediated regulation of nitrogen metabolism in the actinomycete Saccharopolyspora erythraea. Appl Microbiol Biotechnol 98: 7935-7948.