Novel phosphotransferase genes revealed by bacterial genome sequencing: A gene cluster encoding a putative N-acetylgalactosamine metabolic pathway in Escherichia coli

Microbiology

Volumn 142, Issue 2, 1996, Pages 231-250

  Reizer, Jonathan ^a   Ramseier, Tom M ^a   Reizer, Aiala ^a   Charbit, Alain ^a   Saier Jr , Milton H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aldolases; Escherichia coli genome; N acetylgalactosamine; Phosphotransferase system; Sugar transport

Indexed keywords

DEAMINASE; FRUCTOSE BISPHOSPHATE ALDOLASE; N ACETYLGALACTOSAMINE; N ACETYLGLUCOSAMINE; PERMEASE; PHOSPHOTRANSFERASE; REGULATOR PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; CHROMOSOME; ESCHERICHIA COLI; GENE CLUSTER; GENE SEQUENCE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0030064491     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/13500872-142-2-231     Document Type: Article

References (84)

1. Alefounder, P. R. & Perham, R. N. (1989). Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose 1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli. Mol Microbiol 3, 723-732.
2. Alefounder, P. R., Baldwin, D. A., Perham, R. N. & Short, N. J. (1989). Cloning, sequence analysis and over-expression of the gene for the class II fructose 1,6-bisphosphate aldolase of Escherichia coli. Biochem J 257, 529-534.
3. Altamirano, M. M., Plumbridge, J. A. & Calcagno, M. L. (1992). Identification of two cysteine residues forming a pair of vicinal thiols in glucosamine-6-phosphate deaminase from Escherichia coli and a study of their functional role by site-directed mutagenesis. Biochemistry 31, 1153-1158.
4. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
5. von Bodman, B. S., Hayman, G. T. & Farrand, S. K. (1992). Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. Proc Natl Acad Sci USA 89, 643-647.
6. Berry, A. & Marshall, K. E. (1993). Identification of zinc-binding ligands in the class II fructose-1,6-bisphosphate aldolase of Escherichia coli. FEBS Lett 318, 11-16.
7. Boer, H., ten Hoeve-Duurkens, R. H., Schuurman-Wolters, G. K., Dijkstra, A. & Robillard, G. T. (1994). Expression, purification, and kinetic characterization of the mannitol transport domain of the phosphoenolpyruvate-dependent mannitol phosphotransferase system of Escherichia coli. J Biol Chem 269, 17863-17871.
8. Bork, P., Sander, C. & Valencia, A. (1993). Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Prot Sci 2, 31-40.
9. Bork, P., Ouzounis, C., Casari, G., Schneider, R., Sander, C., Dolan, M., Gilbert, W. & Gillevel, P. M. (1995). Exploring the Mycoplasma capricolum genome: a minimal cell reveals its physiology. Mol Microbiol 16, 955-967.
10. Burland, V. D., Plunkett, G., III, Daniels, D. L. & Blattner, F. R. (1993). DNA sequence and analysis of 136 kilobases of the Escherichia coli genome: organizational symmetry around the origin of replication. Genomics 16, 551-561.
11. Burland, V., Plunkett, G., III, Sofia, H. J., Daniels, D. L. & Blattner, F. R. (1995). Analysis of the Escherichia coli genome VI: DNA sequence of the region from 92.8 through 100 minutes. Nucleic Acids Res 23, 2105-2119.
12. Claros, M. G. & von Heijne, G. (1994). TopPred II - an improved software for membrane protein structure predictions. Comp Appl Biosci 10, 685-686.
13. Charbit, A., Reizer, J. & Saier, M. H., Jr (1996). Function of the duplicated IIB domain and oligomeric structure of the fructose permease of E. coli. J Biol Chem (in press).
14. 2 fixation operon of Rhodabacter sphaeroides. J Biol Chem 266, 20447-20452.
15. Choi, Y. L., Kawase, S., Nishida, T., Sakai, H., Komano, T., Kawamukai, M., Utsumi, R., Kohara, Y. & Akiyama, K. (1988). Nucleotide sequence of the glpR gene encoding the repressor for the glycerol-3-phosphate regulon of Escherichia coli K12. Nucleic Acids Res 16, 7732.
16. de Crécy-Lagard, V., Bouvet, O. M. M., Lejeune, P. & Danchin, A. (1991). Fructose catabolism in Xanthomonas campestris pv. campestris. Sequence of the PTS operon, characterization of the fructose-specific enzymes. J Biol Chem 266, 18154-18161.
17. Denisot, M.-A., Le Goffic, F. & Badet, B. (1991). Glucosamine-6-phosphate synthase from Escherichia coli yields two proteins upon limited proteolysis: identification of the glutamine amidohydrolase and 2R ketose/aldose isomerase-bearing domains based on their biochemical properties. Arch Biochem Biophys 288, 225-230.
18. Devereux, J., Haeberli, P. & Smithies, O. (1984). A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12, 387-395.
19. Glc complex of Salmonella typhimurium. Biochemistry 25, 312-318.
20. Erni, B. (1992). Group translocation of glucose and other carbohydrates by the bacterial phosphotransferase system. Int Rev Cytol 137, 127-148.
21. Erni, B., Zanolari, B. & Kocher, H. P. (1987). The mannose permease of Escherichia coli consists of three different proteins. Amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J Biol Chem 262, 5238-5247.
22. Erni, B., Zanolari, B., Graft, P. & Kocher, H. P. (1989). Mannose permease of Escherichia coli. Domain structure and function of the phosphorylating subunit. J Biol Chem 264, 18733-18741.
23. Feng, D.-F. & Doolittle, R. F. (1990). Progressive alignment and phylogenetic tree construction of protein sequences. Methods Enzymol 183, 375-387.
24. Fujita, N., Mori, H., Yura, T. & Ishihama, A. (1994). Systematic sequencing of the Escherichia coli genome: analysis of the 2.4-4.1 min (110,917-193,643 bp) region. Nucleic Acids Res 22, 1637-1639.
25. Gamulin, V., Rinkevich, B., Schäcke, H., Kruse, M., Müller, I. M. & Müller, W. E. G. (1994). Cell adhesion receptors and nuclear receptors are highly conserved from the lowest metazoa (marine sponges) to vertebrates. Biol Chem Hoppe-Seyler 375, 583-588.
26. 2 fixation operon of Rhodobacter spheroids. J Biol Chem 266, 14646-14653.
27. Gutnick, D., Calvo, J. M., Klopotowski, T. & Ames, B. N. (1969). Compounds which serve as the sole source fo carbon or nitrogen for Salmonella typhimurium LT-2. J Bacteriol 100, 215-219.
28. von Heijne, G. (1994). Membrane proteins - from sequence to structure. Annu Rev Biophys Biomol Struct 23, 167-192.
29. Jacobson, G. R. (1992). Interrelationship between protein phosphorylation and oligomerization in transport and chemotaxis via the Escherichia coli mannitol phosphotransferase system. Res Microbiol 143, 113-116.
30. Jacobson, G. R. & Saraceni-Richards, C. (1993). The Escherichia coli mannitol permease as a model for transport via the bacterial phosphotransferase system. J Bioenerg Biomembr 25, 621-626.
31. Komoda, Y., Enomoto, M. & Tominaga, A. (1991). Large inversion in Escherichia coli K-12 1485IN between inversely oriented IS3 elements near lac and cdd. Genetics 129, 639-645.
32. Kruse, M., Mikoc, A., Cetkovic, H., Gamulin, V., Rinkevich, B., Müller, I. M. & Müller, W. E. G. (1994). Cloning of the homeodomain from the marine sponge Geodia cydonium. Mech Ageing Dev 77, 43-54.
33. Kyte, J. & Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J Mol Biol 157, 105-132.
34. Lengeler, J. (1977). Analysis of mutations affecting the dissimilation of galactitol (dulcitol) in Escherichia coli K12. Mol & Gen Genet 152, 83-91.
35. Lengeler, J. W., Jahreis, K. & Wehmeier, U. F. (1994). Enzymes II of the phosphoenolpyruvate-dependent phosphotransferase systems: their structure and function in carbohydrate transport. Biochim Biophys Acta 1188, 1-28.
36. Leonard, J. E. & Saier, M. H., Jr (1983). Mannitol-specific Enzyme II of the bacterial phosphotransferase system II. Reconstitution of vectorial transphosphorylation in phospholipid vesicles. J Biol Chem 258, 10757-10760.
37. Lu, Z. & Lin, E. C. (1989). The nucleotide sequence of Escherichia coli genes for L-fucose dissimilation. Nucleic Acids Res 17, 4883-4884.
38. Marsh, J. J. & Lebherz, H. G. (1992). Fructose-bisphosphate aldolases: an evolutionary history. Trends Biochem Sci 17, 110-113.
39. Martin-Verstraete, I., Debarbouille, M., Klier, A. & Rapoport, G. (1990). Levanase operon of Bacillus subtilis includes a fructose-specific phosphotransferase system regulating the expression of the operon. J Mol Biol 214, 657-671.
40. Meins, M., Jenö, P., Müller, D., Richter, W. J., Rosenbusch, J. P. & Erni, B. (1993). Cysteine phosphorylation of the glucose transporter of Escherichia coli. J Biol Chem 268, 11604-11609.
41. Mitchell, C., Morris, P. W., Lum, L., Spiegelman, G. & Vary, J. C. (1992). The amino acid sequence of a Bacillus subtilis phosphoprotein that matches an orfY-tsr coding sequence. Mol Microbiol 6, 1345-1349.
42. Morse, D. E. & Horecker, B. L. (1968). The mechanism of action of aldolases. Adv Enzymol Relat Areas Mol Biol 31, 125-181.
43. Mutoh, N. & Hayashi, Y. (1994). Molecular cloning and nucleotide sequencing of Schizosaccharomyces pombe homologue of the class II fructose-1,6-bisphosphate aldolase gene. Biochim Biophys Acta 1183, 550-552.
44. Natarajan, K. & Datta, A. (1993). Molecular cloning and analysis of the NAG1 cDNA coding for glucosamine-6-phosphate deaminase from Candida albicans. J Biol Chem 268, 9206-9214.
45. Nobelmann, B. & Lengeler, J. W. (1995). Sequence of the gat operon for galactitol utilization from wild-type strain EC3132 of Escherichia coli. Biochim Biophys Acta 1262, 69-72.
46. Oskouian, B. & Stewart, G. C. (1990). Repression and catabolite repression of the lactose operon of Staphylococcus aureus. J Bacteriol 172, 3804-3812.
47. von der Osten, C. H., Barbas, C. F., III, Wong, C.-H. & Sinskey, A. J. (1989). Molecular cloning, nucleotide sequence and fine-structural analysis of the Corynebacterium glutamicum fda gene: structural comparison of C. glutamicum fructose-1,6-biphosphate aldolase to class I and class II aldolases. Mol Microbiol 3, 1625-1637.
48. Mt1. J Biol Chem 266, 6690-6692.
49. Pearson, W. R. (1994). Using the FASTA program to search protein and DNA sequence databases. In Methods in Molecular Biology: Computer Analysis of Sequence Data, part 2, pp. 365-389. Edited by A. M. Griffin & H. G. Griffin. Totowa, NJ: Humana Press.
50. Pearson, W. R. & Lipman, D. J. (1988). Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85, 2444-2448.
51. Plumbridge, J. A. (1989). Sequence of the nagBACD operon in Escherichia coli K12 and pattern of transcription within the nag regulon. Mol Microbiol 3, 505-515.
52. Plumbridge, J. A., Cochet, O., Souza, J. M., Altamirano, M. M., Calcagno, M. L. & Badet, B. (1993). Coordinated regulation of amino sugar-synthesizing and -degrading enzymes in Escherichia coli K-12. J Bacteriol 175, 4951-4956.
53. Plunkett, G., III, Burland, V., Daniels, D. L. & Blattner, F. R. (1993). Analysis of the Escherichia coli genome. III. DNA sequence of the region from 87.2 to 89.2 minutes. Nucleic Acids Res 21, 3391-3398.
54. Postma, P., Lengeler, J. & Jacobson, G. R. (1993). Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57, 543-594.
55. Rasmussen, S. W. (1994). Sequence of a 28.6 kb region of yeast chromosome XI includes the FBA1 and TOA2 genes, an open reading frame (ORF) similar to a translationally controlled tumor protein, one ORF containing motifs also found in plant storage proteins and 13 ORFs with weak or no homology to known proteins. Yeast S63-68.
56. Reizer, A. & Reizer, J. (1994). Progressive multiple alignment of protein sequences and the construction of phylogenetic trees. In Methods in Molecular Biology: Computer Analysis of Sequence Data, part 2, pp. 319-325. Edited by A. M. Griffin & H. G. Griffin. Totowa, NJ: Humana Press.
57. Reizer, A., Deutscheur, J., Saier, M. H., Jr & Reizer, J. (1991a). Analysis of the gluconate (gnt) operon of Bacillus subtilis. Mol Microbiol 5, 1081-1089.
58. Reizer, A., Pao, G. M. & Saier, M. H., Jr (1991b). Evolutionary relationships among the permease proteins of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. Construction of phylogenetic trees and possible relatedness to proteins of eukaryotic mitochondria. J Mol Evol 33, 179-193.
59. Reizer, J., Michotey, V., Reizer, A. & Saier, M. H., Jr (1994a). Novel phosphotransferase system genes revealed by bacterial genome analysis: unique, putative fructose- and glucoside-specific systems. Prot Sci 3, 3440-3450.
60. Reizer, J., Reizer, A., Kornberg, H. L. & Saier, M. H., Jr (1994b). Sequence of the fruB gene of Escherichia coli encoding the diphosphoryl transfer protein (DTP) of the phosphoenolpyruvate: sugar phosphotransferase system. FEMS Microbiol Lett 118, 159-162.
61. Reizer, J., Reizer, A. & Saier, M. H., Jr (1995). Novel phosphotransferase system genes revealed by bacterial genome analysis - a gene cluster encoding a unique Enzyme I and the proteins of a fructose-like permease system. Microbiology 141, 961-971.
62. Rephaeli, A. W. & Saier, M. H., Jr (1980). Substrate specificity and kinetic characterization of sugar uptake and phosphorylation, catalyzed by the mannose enzyme II of the phosphotransferase system in Salmonella typhimurium. J Biol Chem 255, 8585-8591.
63. Rhiel, E., Flükiger, K., Wehrli, C. & Erni, B. (1994). The mannose transporter of Escherichia coli K12, oligomeric structure, and function of two conserved cysteines. Biol Chem Hoppe-Seyler 375, 551-559.
64. Rogers, M. J.. Ohgi, T., Plumbridge, J. & Söll, D. (1988). Nucleotide sequences of the Escherichia coli nagE and nagB genes: the structural genes for the N-acetylglucosamine transport protein of the bacterial phosphoenolpyruvate:sugar phosphotransferase system and for glucosamine-6-phosphate deaminase. Gene 62, 197-207.
65. van Rooijen, R. J., Dechering, K. J., Niek, C., Wilmink, J. & de Vos, W. M. (1993). Lysines 72, 80 and 213 and aspartic acid 210 of the Lactococcus lactis LacR repressor are involved in the response to the inducer tagatose-6-phosphate leading to induction of lac operon expression. Prot Eng 6, 201-206.
66. Rosey, E. L. & Stewart, G. C. (1992). Nucleotide and deduced amino acid sequences of the lacR, lacABCD, and lacFE genes encoding the repressor, tagatose-6-phosphate gene cluster, and sugar-specific PTS components of the lactose operon of Streptococcus mutans. J Bacteriol 174, 6159-6170.
67. Rosey, E. L., Oskouian, B. & Stewart, G. C. (1991). Lactose metabolism by Staphylococcus aureus: characterization of lacABCD, the structural genes of the tagatose-6-phosphate pathway. J Bacteriol 173, 5992-5998.
68. Saier, M. H., Jr & Leonard, J. E. (1983). The mannitol enzyme II of the bacterial phosphotransferase system: a functionally chimaeric protein with receptor, transport, kinase and regulatory activities. In Multifunctional Proteins: Catalytic/Structural and Regulatory, pp. 11-30. Edited by J. F. Kane. Boca Raton, FL. CRC Press.
69. Saier, M. H., Jr & Reizer, J. (1992). Proposed uniform nomenclature for the proteins and protein domains of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. J Bacteriol 174, 1433-1438.
70. Saier, M. H., Jr & Reizer, J. (1994). The bacterial phosphotransferase system: new frontiers 30 years later. Mol Microbiol 13, 755-764.
71. Schwelberger, H. G., Kohlwein, S. D. & Paltauf, F. (1989). Molecular cloning, primary structure and disruption of the structural gene of aldolase from Saccharomyces cerevisiae. Eur J Biochem 180, 301-308.
72. Sharp, P. M. & Li, W. H. (1987). The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential application. Nucleic Acids Res 15, 1281-1295.
73. Singer, M., Rossmiessl, P., Cali, B. M., Liebke, H. & Gross, C. A. (1991a). The Escherichia coli ts8 mutation is an allele of fda, the gene encoding fructose-1,6-diphosphate aldolase. J Bacteriol 173, 6242-6248.
74. Singer, M., Walter, W. A., Cali, B. M., Rouviere, P., Liebke, H. H., Gourse, R. L. & Gross, C. A. (1991b). Physiological effects of the fructose-1,6-diphosphate aldolase ts8 mutation on stable RNA synthesis in Escherichia coli. J Bacteriol 173, 6249-6257.
75. Smith, D. W. (1988). A complete, yet flexible, system for DNA/protein sequence analysis using VAX/VMS computers. Comput Appl Biosci 4, 212.
76. Smith, M. W., Feng, D.-F. & Doolittle, R. F. (1992). Evolution by acquisition: the case for horizontal gene transfers. Trends Biochem Sci 17, 489-493.
77. Man subunit. J Biol Chem 268, 27094-27099.
78. Trach, K., Chapman, J. W., Piggot, P., LeCoq, D. & Hoch, J. A. (1988). Complete sequence and transcriptional analysis of the spoOF region of the Bacillus subtilis chromosome. J Bacteriol 170, 4194-4208.
79. Valentin-Hansen, P., Hojrup, P. & Short, S. (1985). The primary structure of the DeoR repressor from Escherichia coli K-12. Nucleic Acids Res 13, 5927-5936.
80. de Vos, W. M. Boerrigter, I. J., van Rooyen, R. J., Reiche, B. & Hengstenberg, W. (1990). Characterization of the lactose-specific enzymes of the phosphotransferase system in Lactococcus lactis. J Biol Chem 265, 22554-22560.
81. Wehmeier, U. F. & Lengeler, J. W. (1994). Sequence of the sor operon for L-sorbose utilization from Klebsiella pneumoniae KAY2026. Biochim Biophys Acta 1208, 348-351.
82. Wehmeier, U. F., Wöhrl, B. M. & Lengeler, J. W. (1995). Molecular analysis of the phosphoenolpyruvate-dependent L-sorbose: phosphotransferase system from Klebsiella pneumoniae and of its multidomain structure. Mol & Gen Genet 246, 610-618.
83. Wilson, R. and others (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368, 32-38.
84. Yamada, M. & Saier, M. H., Jr (1988). Positive and negative regulators for glucitol (gut) operon expression in Escherrchia coli. J Mol Biol 203, 569-583.