1887

Abstract

Summary: We have analysed a gene cluster in the 67.4-76.0 min region of the chromosome, revealed by recent systematic genome sequencing. The genes within this cluster include: (1) five genes encoding homologues of the mannose permease of the phosphotransferase system (IIB, IIB', IIC, IIC' and IID); (2) genes encoding a putative -acetylgalactosamine 6-phosphate metabolic pathway including (a) a deacetylase, (b) an isomerizing deaminase, (c) a putative carbohydrate kinase, and (d) an aldolase; and (3) a transcriptional regulatory protein homologous to members of the DeoR family. Evidence is presented suggesting that the aldolase-encoding gene within this cluster is the previously designated gene that encodes tagatose-1,6-bisphosphate aldolase. These proteins and a novel IIA-like protein encoded in the 2.4-4.1 min region are characterized with respect to their sequence similarities and phylogenetic relationships with other homologous proteins. A pathway for the metabolism of -acetylgalactosamine biochemically similar to that for the metabolism of -acetylglucosamine is proposed.

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1996-02-01
2021-08-05
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References

  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. Mot Microbiol 3:723–732
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  4. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mot Biol 215:403–410
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  8. Bork P., Sander C., Valencia A. 1993; Convergent evolution of similar enzymatic function on different protein folds: the hexo-kinase, ribokinase, and galactokinase families of sugar kinases. Prot Sci 2:31–40
    [Google Scholar]
  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. Mot Microbiol 16:955–967
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  12. Claros M. G., von Heijne G. 1994; TopPred II - an improved software for membrane protein structure predictions. Comp Appl Biosci 10:685–686
    [Google Scholar]
  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
    [Google Scholar]
  14. Chen J. H., Gibson J. L., McCue L. A., Tabita F. R. 1991; Identification, expression, and deduced primary structure of transketolase and other enzymes encoded within the form II COa fixation operon of Rhodobacter sphaeroides. J Biol Chem 266:20447–20452
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  18. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
    [Google Scholar]
  19. Erni B. 1986; Glucose-specific permease of the bacterial phosphotransferase system: phosphorylation and oligomeric structure of the glucose-specific IIGlc-IIIGlc complex of Salmonella typhimurium. Biochemistry 25:312–318
    [Google Scholar]
  20. Erni B. 1992; Group translocation of glucose and other carbohydrates by the bacterial phosphotransferase system. Int Rev Cytol 137:127–148
    [Google Scholar]
  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
    [Google Scholar]
  22. Erni B., Zanolari B., Graff P., Kocher H. P. 1989; Mannose permease of Escherichia coli. Domain structure and function of the phosphorylating subunit. J Biol Chem 264:18733–18741
    [Google Scholar]
  23. Feng D.-F., Doolittle R. F. 1990; Progressive alignment and phylogenetic tree construction of protein sequences. Methods En^ymol 183:375–387
    [Google Scholar]
  24. Fujita N., Mori H., Yura T., Ishihama A. 1994; Systematic sequencing of the Escherichia coli genome: analysis of the 24-4-1 min (110,917-193,643 bp) region. Nucleic Acids Res 22:1637–1639
    [Google Scholar]
  25. Gamulin V., Rinkevich B., Schacke H., Kruse M., Mailer I. M., Mtlller 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
    [Google Scholar]
  26. Gibson J. L., Falcone D. L., Tabita F. R. 1991; Nucleotide sequence, transcriptional analysis, and expression of genes encoded within the form I COa fixation operon of Rhodobacter spheroids. J Biol Chem 266:14646–14653
    [Google Scholar]
  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
    [Google Scholar]
  28. von Heijne G. 1994; Membrane proteins - from sequence to structure. Annu Rev Biophys Biomol Struct 23:167–192
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  32. Kruse M., Mikoc A., Cetkovic H., Gamulin V., Rinkevich B., Muller I. M., Muller W. E. G. 1994; Cloning of the homeo-domain from the marine sponge Geodia cydonium. Mech Ageing Dev 77:43–54
    [Google Scholar]
  33. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. J Mot Biol 157:105–132
    [Google Scholar]
  34. Lengeler J. 1977; Analysis of mutations affecting the dissimilation of galactitol (dulcitol) in Escherichia coli K12. Mot & Gen Genet 152:83–91
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  37. Lu Z., Lin E. C. 1989; The nucleotide sequence of Escherichia coli genes for L-fucose dissimilation. Nucleic Acids Res 17:4883–4884
    [Google Scholar]
  38. Marsh J. J., Lebherz H. G. 1992; Fructose-bisphosphate aldolases: an evolutionary history. Trends Biochem Sci 17:110–113
    [Google Scholar]
  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 Mot Biol 214:657–671
    [Google Scholar]
  40. Meins M., Jend P., Muller 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
    [Google Scholar]
  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. Mot Microbiol 6:1345–1349
    [Google Scholar]
  42. Morse D. E., Horecker B. L. 1968; The mechanism of action of aldolases. Adv Enzymol Relat Areas Mot Biol 31:125–181
    [Google Scholar]
  43. Mutoh N., Hayashi Y. 1994; Molecular cloning and nucleotide sequencing of Schi^psaccharomyces pombe homologue of the class II fructose-1,6-bisphosphate aldolase gene. Biochim Biophys Acta 1183:550–552
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  46. Oskouian B., Stewart G. C. 1990; Repression and catabolite repression of the lactose operon of Staphylococcus aureus. J Bacteriol 172:3804–3812
    [Google Scholar]
  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. Mot Microbiol 3:1625–1637
    [Google Scholar]
  48. Pas H. H., Meyer G. H., Kruizinga W. H., Tamminga K. S., van Weeghel R. P., Robillard G. T. 1991; Phospho-NMR demonstration of phosphocysteine as a catalytic intermediate on the Escherichia coli phosphotransferase system EIIMtl. J Biol Chem 266:6690–6692
    [Google Scholar]
  49. Pearson W. R. 1994; Using the fasta program to search protein and DNA sequence databases. Methods in Molecular Biology: Computer Analysis of Sequence Datapart 2365–389 Edited by Griffin A. M., Griffin H. G. Totowa, NJ: Humana Press;
    [Google Scholar]
  50. Pearson W. R., Lipman D. J. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  54. Postma P., Lengeler J., Jacobson G. R. 1993; Phosphoenolpyruvate : carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57:543–594
    [Google Scholar]
  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. YeastS63–68
    [Google Scholar]
  56. Reizer A., Reizer J. 1994; Progressive multiple alignment of protein sequences and the construction of phylogenetic trees. Methods in Molecular Biology: Computer Analysis of Sequence Datapart 2319–325 Edited by Griffin A. M., Griffin H. G. Totowa, NJ: Humana Press;
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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. Proc Sci 3:3440–3450
    [Google Scholar]
  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
    [Google Scholar]
  61. Reizer J., Reizer A., Saier M. H. Jr 1995; Novel phosphot ransferase 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
    [Google Scholar]
  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
    [Google Scholar]
  63. Rhiel E., Flukiger 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
    [Google Scholar]
  64. Rogers M. J., Ohgi T., Plumbridge J., Soli 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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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. Multifunctional Proteins: Catalytic/Structural and Regulatory11–30 Edited by Kane J. F. Boca Raton, FL: CRC Press;
    [Google Scholar]
  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
    [Google Scholar]
  70. Saier M. H. Jr, Reizer J. 1994; The bacterial phosphotransferase system: new frontiers 30 years later. Mol Microbiol 13:755–764
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  73. Singer M., Rossmiessl P., Cali B. M., Liebke H., Gross C. A. 1991a; The Escherichia coli ts8 mutation is an allele offda, the gene encoding fructose-1,6-diphosphate aldolase. J Bacteriol 173:6242–6248
    [Google Scholar]
  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
    [Google Scholar]
  75. Smith D. W. 1988; A complete, yet flexible, system for DNA/protein sequence analysis using VAX/VMS computers. Comput Appl Biosci 4:212
    [Google Scholar]
  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
    [Google Scholar]
  77. Stolz B., Huber M., Markovic-Housley Z., Erni B. 1993; The mannose transporter of Escherichia coli. Structure and function of the IIABMan subunit. J Biol Chem 268:27094–27099
    [Google Scholar]
  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 BacIIIus subtilis chromosome. J Bacteriol 170:4194–4208
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  82. Wehmeier U. F., Wohrl 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
    [Google Scholar]
  83. Wilson R. others 1994; 2-2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368:32–38
    [Google Scholar]
  84. Yamada M., Saier M. H. Jr 1988; Positive and negative regulators for glucitol (gut) operon expression in Escherichia coli. J Mol Biol 203:569–583
    [Google Scholar]
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