Ammonium assimilation and nitrogen control in Corynebacterium glutamicum and its relatives: An example for new regulatory mechanisms in actinomycetes

FEMS Microbiology Reviews

Volumn 27, Issue 5, 2003, Pages 617-628

  Burkovski, Andreas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Ammonium assimilation; Corynebacterium glutamicum; Mycobacterium; Nitrogen control; Streptomyces

Indexed keywords

AMMONIA; AMMONIUM DERIVATIVE; BACTERIAL PROTEIN; HEXOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; NITROGEN; NUCLEIC ACID; REPRESSOR PROTEIN; SYNTHETASE;

ACTINOBACTERIA; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BACTERIAL METABOLISM; CELL METABOLISM; CORYNEBACTERIUM DIPHTHERIAE; CORYNEBACTERIUM EFFICIENS; CORYNEBACTERIUM GLUTAMICUM; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE EXPRESSION; GENE SEQUENCE; GRAM POSITIVE BACTERIUM; MACROMOLECULE; MOLECULAR MODEL; MYCOBACTERIUM; NITROGEN METABOLISM; NONHUMAN; PROKARYOTE; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SOIL MICROFLORA; STREPTOMYCETACEAE;

ACTINOBACTERIA (CLASS); BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; CORYNEBACTERIUM; CORYNEBACTERIUM DIPHTHERIAE; CORYNEBACTERIUM EFFICIENS; CORYNEBACTERIUM GLUTAMICUM; ESCHERICHIA COLI; MYCOBACTERIUM; POSIBACTERIA; PROKARYOTA; STREPTOMYCES; STREPTOMYCINEAE;

EID: 0345447496     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-6445(03)00067-6     Document Type: Review

References (89)

1. Lehmann, K.B. and Neumann, R. (1896) Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik. J.F. Lehmann, Munich.
2. http://www.dsmz.de/bactnom/nam0942.htm : Bacterial nomenclature up-to-date, genus Corynebacterium. Deutsche Sammlung für Mikroorganismen und Zellkulturen, Braunschweig.
3. Stackebrandt E., Rainey F.A., Ward-Rainey N.L. Proposal for a new hierachic classification system, Actinobacteria classis nov. Int. J. Syst. Bacteriol. 47:1997;97-102.
4. Kinoshita S., Udaka S., Shimono M. Amino acid fermentation. I. Production of L-glutamic acid by various microorganisms. J. Gen. Appl. Microbiol. 3:1959;193-205.
5. Udaka S. Screening method for microorganisms accumulating metabolites and its use in the isolation of Micrococcus glutamicus. J. Bacteriol. 79:1960;745-755.
6. Eggeling L., Sahm H. The cell wall barrier of Corynebacterium glutamicum and amino acid efflux. J. Biosci. Bioeng. 92:2001;201-213.
7. Burkovski A. I do it my way: Regulation of ammonium uptake and ammonium assimilation in Corynebacterium glutamicum. Arch. Microbiol. 179:2003;83-88.
8. + transport systems. In: Alkali Cation Transport Systems in Prokaryotes (Bakker, E.P., Ed.), pp. 379-395. CRC Press, Boca Raton, FL.
9. Soupene E., He L., Yan D., Kustu S. Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc. Natl. Acad. Sci. USA. 95:1998;7030-7034.
10. 3 bidirectionally. Proc. Natl. Acad. Sci. USA. 99:2002;3926-3931.
11. Merrick M., Edwards R.A. Nitrogen control in bacteria. Microbiol. Rev. 59:1995;604-622.
12. II signal transduction proteins. Trends Microbiol. 8:2000;172-179.
13. II signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol. Mol. Biol. Rev. 65:2001;80-105.
14. II protein. Biochemistry. 37:1998;12782-12794.
15. Jiang P., Peliska J.A., Ninfa A.J. Reconstitution of the signal-transduction bicyclic cascade responsible for the regulation of Ntr gene transcription in Escherichia coli. Biochemistry. 37:1998;12795-12801.
16. Jiang P., Peliska J.A., Ninfa A.J. The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry. 37:1998;12802-12810.
17. Bueno R., Pahel G., Magasanik B. Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli. J. Bacteriol. 164:1985;816-822.
18. II protein and nucleotide sequence of its structural gene. J. Biol. Chem. 262:1987;8690-8695.
19. II in Escherichia coli: a new regulatory protein in the glutamine synthetase cascade. FEMS Microbiol. Lett. 132:1995;153-157.
20. II protein in the regulation of glutamine synthetase in Escherichia coli. Mol. Microbiol. 21:1996;133-146.
21. II- mediated signal transduction systems. Mol. Microbiol. 33:1999;338-349.
22. II (GlnB) and GlnK form heterotrimers in vivo: Fine tuning of the nitrogen signal cascade. Proc. Natl. Acad. Sci. USA. 97:2000;3942-3947.
23. II and GlnK signal transduction proteins in Escherichia coli. J. Bacteriol. 184:2002;5364-5375.
24. Coutts G., Thomas G., Blakey D., Merrick M. Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J. 21:2002;536-545.
25. Fisher S.H. Regulation of nitrogen metabolism in Bacillus subtilis: vive la différence! Mol. Microbiol. 32:1999;223-232.
26. Belitsky B.R., Wray L.V. Jr., Fisher S.H., Bohannon D.E., Sonenshein A.L. Role of TnrA in nitrogen source-dependent repression of Bacillus subtilis glutamate synthase gene expression. J. Bacteriol. 182:2000;5939-5947.
27. Wray L.V., Zalieckas J.M., Fisher S.H. Bacillus subtilis glutamine synthetase controls gene expression through a protein-protein interaction with transcription factor TnrA. Cell. 107:2001;427-435.
28. Ratnayake-Lecamwasam M., Serror P., Wong K.-W., Sonenshein A.L. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 15:2001;1093-1103.
29. Marini A.M., Vissers S., Urrestarazu A., André B. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J. 13:1994;3456-3463.
30. Siewe R.M., Weil B., Burkovski A., Eikmanns B.J., Eikmanns M., Krämer R. Functional and genetic characterization of the (methyl)ammonium uptake carrier of Corynebacterium glutamicum. J. Biol. Chem. 271:1996;5398-5403.
31. Meier-Wagner J., Nolden L., Jakoby M., Siewe R., Krämer R., Burkovski A. Multiplicity of ammonium uptake systems in Corynebacterium glutamicum: Role of Amt and AmtB. Microbiology. 147:2001;135-143.
32. Jakoby M., Krämer R., Burkovski A. Nitrogen regulation in Corynebacterium glutamicum: Isolation of genes involved and biochemical characterization of corresponding proteins. FEMS Microbiol. Lett. 173:1999;303-310.
33. Jakoby M., Nolden L., Meier-Wagner J., Krämer R., Burkovski A. AmtR, a global repressor in the nitrogen regulation system of Corynebacterium glutamicum. Mol. Microbiol. 37:2000;964-977.
34. 15N nuclear magnetic resonance. Appl. Environ. Microbiol. 65:1999;1099-1109.
35. Reitzer, L.J. and Magasanik, B. (1987) Ammonium assimilation and the biosynthesis of glutamine, glutamate, aspartate, asparagine, L-alanine, and D-alanine. In: Escherichia coli and Salmonella (Neidthardt, E.C., Ingraham, J.L., Magasanik, B., Schaechter, M. and Umbarger, H.E., Eds.), pp. 302-320. American Society of Microbiology, Washington, DC.
36. Kimura K. The significance of glutamic dehydrogenase in glutamic acid fermentation. J. Gen. Appl. Microbiol. 8:1962;253-260.
37. Oshima K., Tanaka K., Kinoshita S. Studies on glutamic acid fermentation. XI. Purification and properties of L-glutamic acid dehydrogenase from Micrococcus glutamicus. Agric. Biol. Chem. 28:1964;714-722.
38. Shiio I., Ozaki H. Regulation of nicotinamide adenine dinucleotide phosphate-specific glutamate dehydrogenase from Brevibacterium flavum, a glutamate-producing bacterium. J. Biochem. 68:1970;633-647.
39. T to Corynebacterium glutamicum and their distinction by rRNA gene restriction patterns. Int. J. Syst. Bacteriol. 41:1991;255-260.
40. Börmann E.R., Eikmanns B.J., Sahm H. Molecular analysis of the Corynebacterium glutamicum gdh gene encoding glutamate dehydrogenase. Mol. Microbiol. 6:1992;317-326.
41. Börmann-El Kholy E.R., Eikmanns B.J., Gutmann M., Sahm H. Glutamate dehydrogenase is not essential for glutamate formation in Corynebacterium glutamicum. Appl. Environ. Microbiol. 59:1993;2329-2331.
42. Tesch M., Eikmanns B.J., de Graaf A.A., Sahm H. Ammonia assimilation in Corynebacterium glutamicum and a glutamate dehydrogenase-deficient mutant. Biotechnol. Lett. 20:1998;953-957.
43. Sung H.A., Tachiki T., Kumagai H., Tochikura T. Production and preparation of glutamate synthase from Brevibacterium flavum. J. Ferment. Technol. 62:1984;569-575.
44. Shiio I., Ujigawa K. Enzymes of the glutamate and aspartate synthetic pathways in glutamate-producing Brevibacterium flavum. J. Biochem. 84:1978;647-657.
45. Tochikura T., Sung H.-C., Tachiki T., Kumagai H. Occurrence of glutamate synthase in Brevibacterium flavum. Agric. Biol. Chem. 48:1984;2149-2150.
46. Sung H.A., Tamaki H., Tachiki T., Kumagai H., Tochikura T. Ammonia assimilation by glutamine synthase/glutamate synthase system in Brevibacterium flavum. J. Ferment. Technol. 63:1985;5-10.
47. Jakoby M., Tesch M., Sahm H., Krämer R., Burkovski A. Isolation of the Corynebacterium glutamicum glnA gene encoding glutamine synthetase I. FEMS Microbiol. Lett. 154:1997;81-88.
48. Beckers G., Nolden L., Burkovski A. Glutamate synthase of Corynebacterium glutamicum is not essential for glutamate synthesis and is regulated by the nitrogen status. Microbiology. 147:2001;2961-2970.
49. Schulz A.A., Collett H.J., Reid S.J. Regulation of glutamine synthetase and glutamate synthase in Corynebacterium glutamicum ATCC 13032. FEMS Microbiol. Lett. 205:2002;361-367.
50. Brown J.R., Masuchi Y., Robb F.T., Doolittle W.F. Evolutionary relationships of bacterial and archaeal glutamine synthetases. J. Mol. Evol. 38:1994;566-576.
51. Nolden L., Farwick M., Krämer R., Burkovski A. Glutamine synthetases in Corynebacterium glutamicum: transcriptional control and regulation of activity. FEMS Microbiol. Lett. 201:2001;91-98.
52. Faires N., Tobisch S., Bachem S., Martin-Verstraete I., Hecker M., Stülke J. The catabolite control protein CcpA controls ammonium assimilation in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 1:1999;141-148.
53. Helling R.B. Why does Escherichia coli have two primary pathways for synthesis of glutamate? J. Bacteriol. 176:1994;4664-4668.
54. Goss T.J., Perez-Matos A., Bender R.A. Roles of glutamate synthase, gltBD, and gltF in nitrogen metabolism of Escherichia coli and Klebsiella aerogenes. J. Bacteriol. 183:2001;6607-6619.
55. Nolden L., Ngouoto-Nkili C.-E., Bendt A.K., Krämer R., Burkovski A. Sensing nitrogen limitation in Corynebacterium glutamicum: The role of glnK and glnD. Mol. Microbiol. 42:2001;1281-1295.
56. Hesketh A., Fink D., Gust B., Rexer H.U., Scheel B., Chater K., Wohlleben W., Engels A. The GlnD and GlnK homologues of Streptomyces coelicolor A3 are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol. Microbiol. 46:(2):2002;319-330.
57. Krämer R., Lambert C. Uptake of glutamate in Corynebacterium glutamicum. 2. Evidence for a primary active transport system. Eur. J. Biochem. 194:1990;937-944.
58. Ikeda T.P., Shauger A.E., Kustu S. Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. J. Mol. Biol. 259:1996;589-607.
59. Schmitz R.A. Internal glutamine and glutamate pools in Klebsiella pneumoniae grown under different conditions of nitrogen availability. Curr. Microbiol. 41:2000;357-362.
60. Hu P., Leighton T., Ishkhanova G., Kustu S. Sensing of nitrogen limitation by Bacillus subtilis: comparison to enteric bacteria. J. Bacteriol. 181:1999;5042-5050.
61. Oguiza J.A., Marcos A.T., Malumbres M., Martin J.F. Multiple sigma factor genes in Brevibacterium lactofermentum: characterization of sigA and sigB. J. Bacteriol. 178:1996;550-553.
62. Halgasova N., Bukovska G., Timko J., Kormanec J. Cloning and transcriptional characterization of two sigma factor genes, sigA and sigB, from Brevibacterium flavum. Curr. Microbiol. 43:2001;249-254.
63. Halgasova N., Bukovska G., Ugorcakova J., Timko J., Kormanec J. The Brevibacterium flavum sigma factor SigB has a role in the environmental stress response. FEMS Microbiol. Lett. 216:2002;77-84.
64. Nolden L., Beckers G., Burkovski A. Nitrogen assimilation in Corynebacterium diphtheriae: pathways and regulatory cascades. FEMS Microbiol. Lett. 208:2002;287-293.
65. Fudou R., Jojima Y., Seto A., Yamada K., Rimura E., Nakamatsu T., Hirashi A., Yamanaka S. Corynebacterium efficiens sp. nov., a glutamic-acid-producing species from soil and plant material. Int. J. Syst. Evol. Microbiol. 52:2002;1127-1131.
66. http://www3.bio.nite.go.jp./cgi-bin/dogan/genome-top.cgi ?′ce′.
67. Harth G., Horwitz M.A. Expression and efficient export of enzymatically active Mycobacterium tuberculosis glutamine synthetase in Mycobacterium smegmatis and evidence that the information for export is contained within the protein. J. Biol. Chem. 272:1997;22728-22735.
68. Harth G., Clemens D.L., Horwitz M.A. Glutamine synthetase of Mycobacterium tuberculosis: extracellular release and characterization of its enzymatic activity. Proc. Natl. Acad. Sci. USA. 91:1994;9342-9346.
69. Harth G., Horwitz M.A. An inhibitor of exported Mycobacterium tuberculosis glutamine synthetase selectively blocks the growth of pathogenic mycobacteria in axenic culture and in human monocytes: extracellular proteins as potential novel drug targets. J. Exp. Med. 189:1999;1425-1436.
70. Harth G., Zamecnik P.C., Tang J.Y., Tabatadze D., Horwitz M.A. Treatment of Mycobacterium tuberculosis with antisense oligonucleotides to glutamine synthetase mRNA inhibits glutamine synthetase activity, formation of the poly-L-glutamate/glutamine cell wall structure, and bacterial replication. Proc. Natl. Acad. Sci. USA. 97:2000;418-423.
71. Harth G., Horwitz M.A. Inhibition of Mycobacterium tuberculosis glutamine synthetase as a novel antibiotic strategy against tuberculosis: demonstration of efficacy in vivo. Infect. Immun. 71:2003;456-464.
72. Parish T., Stoker N.G. glnE is an essential gene in Mycobacterium tuberculosis. J. Bacteriol. 182:2000;5715-5720.
73. Dandekar T., Snel B., Huynen M., Bork P. Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem. Sci. 23:1998;324-328.
74. Cole S.T., Eiglmeier K., Parkhill J., James K.D., Thomson N.R., Wheeler P.R., Honoré N., Garnier T., Churcher C., Harris D., Mungall K., Basham D., Brown D., Chillingworth T., Connor R., Davies R.M., Devlin K., Duthoy S., Feltwell T., Fraser A., Hamlin N., Holroyd S., Hornsby T., Jagels K., Lacroix C., Maclean J., Moule S., Murphy L., Oliver K., Quail M.A., Rajandream M.-A., Rutherford K.M., Rutter S., Seeger K., Simon S., Simmonds M., Skelton J., Squares R., Squares S., Stevens K., Taylor K., Whitehead S., Woodward J.R., Barrell B.G. Massive gene decay in the leprosy bacillus. Nature. 409:2001;1007-1011.
75. Vissa, V.D. and Brennan, P.J. (2001) The genome of Mycobacterium leprae: a minimal mycobacterial gene set. http://genomebiology.com/2001/2/8/reviews/ 1023.1 .
76. Fisher S.H. Glutamate synthesis in Streptomyces coelicolor. J. Bacteriol. 171:1989;2372-2377.
77. Weischuh N., Fink D., Vierling S., Bibb M.J., Wohlleben W., Engels A. Transcriptional analysis of the gene for glutamine synthetase II and two upstream genes in Streptomyces coelicolor A3. Mol. Gen. Genet. 264:(2):2000;461-469.
78. Bentley S.D., Chater K.F., Cerdeno-Tárraga A.-M., Challis G.L., Thomson N.R., James K.D., Harris D.E., Quail M.A., Kieser H., Harper D., Bateman A., Brown S., Chandra G., Chen C.W., Collins M., Cronin A., Fraser A., Goble A., Hidalgo J., Hornsby T., Howarth S., Huang C.-H., Kieser T., Larke L., Murphy L., Oliver K., O'Neil S., Rabbinowitsch E., Rajandream M.A., Rutherford K., Rutter S., Seeger K., Saunders D., Sharp S., Squares R., Squares S., Taylor K., Warren T., Wietzorrek A., Woodward J., Barell B.G., Parkhill J., Hopwood D.A. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3. Nature. 417:(2):2002;141-147.
79. Fink D., Weischuh N., Reuther J., Wohlleben W., Engels A. Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3. Mol. Microbiol. 46:(2):2002;331-347.
80. Fink D., Falke D., Wohlleben W., Engels A. Nitrogen metabolism in Streptomyces coelicolor A3: modification of glutamine synthetase I by an adenylyltransferase. Microbiology. 145:(2):1999;2313-2322.
81. Hillemann D., Dammann T., Hillemann A., Wohlleben W. Genetic and biochemical characterization of the two glutamine synthetases GSI and GSII of the phosphinothricyl-alanyl-alanine producer, Streptomyces viridochromogenes Tu494. J. Gen. Microbiol. 139:1993;1773-1783.
82. Wray L.V. Jr., Fisher S.H. The Streptomyces coelicolor glnR gene encodes a protein similar to other bacterial response regulators. Gene. 16:1993;145-150.
83. Chater, K.F. and Losick, R. (1996) The mycelial life style of Streptomyces coelicolor A3(2) and its relatives. In: Bacteria as Multicellular Organisms (Shapiro, J.H. and Dworkin, M., Eds.), pp. 93-114. Oxford University Press.
84. Hermann T., Pfefferle W., Baumann C., Busker E., Schaffer S., Bott M., Sahm H., Dusch N., Kalinowski J., Pühler A., Bendt A.K., Krämer R., Burkovski A. Proteome analysis of Corynebacterium glutamicum. Electrophoresis. 22:2001;1712-1723.
85. Schaffer S., Weil B., Nguyen V.D., Dongmann G., Gunther K., Nickolaus M., Hermann T., Bott M. A high-resolution reference map for cytoplasmic and membrane-associated proteins of Corynebacterium glutamicum. Electrophoresis. 22:2001;4404-4422.
86. Schmid R., Uhlemann E.-M., Nolden L., Wersch G., Hecker R., Hermann T., Marx A., Burkovski A. Response to nitrogen starvation in Corynebacterium glutamicum. FEMS Microbiol. Lett. 187:2000;83-88.
87. Kronemeyer W., Peekhaus N., Krämer R., Sahm H., Eggeling L. Structure of the gluABCD cluster encoding the glutamate uptake system of Corynebacterium glutamicum. J. Bacteriol. 177:1995;1152-1158.
88. Nolden L., Beckers G., Möckel B., Pfefferle W., Nampoothiri K.M., Krämer R., Burkovski A. Urease of Corynebacterium glutamicum: organisation of corresponding genes and investigation of activity. FEMS Microbiol. Lett. 189:2000;305-310.
89. Pukás L.G., Inui M., Yukawa H. Structure of the urease operon of Corynebacterium glutamicum. DNA Seq. 11:2000;383-394.