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Volume 155, Issue 2

Roles of maltodextrin and glycogen phosphorylases in maltose utilization and glycogen metabolism in Free

Abstract

transiently accumulates large amounts of glycogen, when cultivated on glucose and other sugars as a source of carbon and energy. Apart from the debranching enzyme GlgX, which is required for the formation of maltodextrins from glycogen, -glucan phosphorylases were assumed to be involved in glycogen degradation, forming -glucose 1-phosphate from glycogen and from maltodextrins. We show here that in fact possesses two -glucan phosphorylases, which act as a glycogen phosphorylase (GlgP) and as a maltodextrin phosphorylase (MalP). By chromosomal inactivation and subsequent analysis of the mutant, was identified as the gene. The deletion mutant Δ completely lacked MalP activity and showed reduced intracellular glycogen degradation, confirming the proposed pathway for glycogen degradation in via GlgP, GlgX and MalP. Surprisingly, the Δ mutant showed impaired growth, reduced viability and altered cell morphology on maltose and accumulated much higher concentrations of glycogen and maltodextrins than the wild-type during growth on this substrate, suggesting an additional role of MalP in maltose metabolism of . Further assessment of enzyme activities revealed the presence of 4--glucanotransferase (MalQ), glucokinase (Glk) and -phosphoglucomutase (-Pgm), and the absence of maltose hydrolase, maltose phosphorylase and -Pgm, all three known to be involved in maltose utilization by Gram-positive bacteria. Based on these findings, we conclude that metabolizes maltose via a pathway involving maltodextrin and glucose formation by MalQ, glucose phosphorylation by Glk and maltodextrin degradation via the reactions of MalP and -Pgm, a pathway hitherto known to be present in Gram-negative rather than in Gram-positive bacteria.

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Keyword(s): cell dw, cell dry weight and WT, wild-type
SGM
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2009-02-01
2024-04-18
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References

  1. Adhya S., Schwartz M. 1971; Phosphoglucomutase mutants of Escherichia coli K-12. J Bacteriol 108:621–626
     [Google Scholar]
  2. Alonso-Casajus N., Dauvillee D., Viale A. M., Munoz F. J., Baroja-Fernandez E., Moran-Zorzano M. T., Eydallin G., Ball S., Pozueto-Romero J. 2006; Glycogen phosphorylase, the product of the glgP gene, catalyzes glycogen breakdown by removing glucose units from the nonreducing ends in Escherichia coli . J Bacteriol 188:5266–5272
     [Google Scholar]
  3. 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
     [Google Scholar]
  4. Andersson U., Radström P. 2002; β -Glucose 1-phosphate-interconverting enzymes in maltose- and trehalose-fermenting lactic acid bacteria. Environ Microbiol 4:81–88
     [Google Scholar]
  5. Bibel M., Brettl C., Gosslar U., Kriegshäuser G., Liebl W. 1998; Isolation and analysis of genes for amylolytic enzymes of the hyperthermophilic bacterium Thermotoga maritima . FEMS Microbiol Lett 158:9–15
     [Google Scholar]
  6. Blombach B., Schreiner M. E., Moch M., Oldiges M., Eikmanns B. J. 2007; Effect of pyruvate dehydrogenase complex deficiency on l-lysine production with Corynebacterium glutamicum . Appl Microbiol Biotechnol 76:615–623
     [Google Scholar]
  7. Boos W., Shuman H. 1998; Maltose/maltodextrin system of Escherichia coli : transport, metabolism, and regulation. Microbiol Mol Biol Rev 62:204–229
     [Google Scholar]
  8. Chen J., Lu G., Lin J., Davidson A. L., Quiocho F. A. 2003; A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol Cell 12:651–661
     [Google Scholar]
  9. Cho H. Y., Kim Y. W., Kim T. J., Lee H. S., Kim D. Y., Kim J. W., Lee Y. W., Leed S., Park K. H. 2000; Molecular characterization of a dimeric intracellular maltogenic amylase of Bacillus subtilis SUH4–2. Biochim Biophys Acta 1478:333–340
     [Google Scholar]
  10. Daus M. L., Landmesser H., Schlosser A., Müller P., Hermann A., Schneider E. 2006; ATP induces conformational changes of periplasmatic loop regions of the maltose ATP-binding cassette transporter. J Biol Chem 281:3856–3865
     [Google Scholar]
  11. Dauvillee D., Kinderf I. S., Zhongyi L., Kosar-Hashemi B., Samuel M. S., Rampling L., Ball S., Morell M. K. 2005; Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187:1465–1473
     [Google Scholar]
  12. De Smet K. A. L., Weston A., Brown I. N., Young D. B., Robertson B. D. 2000; Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146:199–208
     [Google Scholar]
  13. Dippel R., Bergmiller T., Böhm A., Boos W. 2005; The maltodextrin system of Escherichia coli : glycogen-derived endogenous induction and osmoregulation. J Bacteriol 187:8332–8339
     [Google Scholar]
  14. Dominguez H., Rollin C., Guyonvarch A., Guerquin-Kern J.-L., Cocaign-Bousquet M., Lindley N. D. 1998; Carbon-flux distribution in the central metabolic pathways of Corynebacterium glutamicum during growth on fructose. Eur J Biochem 254:96–102
     [Google Scholar]
  15. Dower W. J., Miller J. F., Ragsdale C. W. 1988; High efficiency transformation of Escherichia coli by high voltage electroporation. Nucleic Acids Res 16:6127–6145
     [Google Scholar]
  16. Eggeling L., Bott M. 2005 Handbook of Corynebacterium glutamicum Boca Raton, FL: CRC Press;
  17. Ehrmann M. A., Vogel R. F. 1998; Maltose metabolism of Lactobacillus sanfrancensis : cloning and heterologous expression of the key enzymes, maltose phosphorylase and phosphoglucomutase. FEMS Microbiol Lett 169:81–86
     [Google Scholar]
  18. Eikmanns B. J., Kleinertz E., Liebl W., Sahm H. 1991a; A family of Corynebacterium glutamicum / Escherichia coli shuttle vectors for cloning, controlled gene expression, and promoter probing. Gene 102:93–98
     [Google Scholar]
  19. Eikmanns B. J., Metzger M., Reinscheid D., Kircher M., Sahm H. 1991b; Amplification of three threonine biosynthesis genes in Corynebacterium glutamicum and its influence on carbon flux in different strains. Appl Microbiol Biotechnol 34:617–622
     [Google Scholar]
  20. Eikmanns B. J., Thum-Schmitz N., Eggeling L., Ludtke K. U., Sahm H. 1994; Nucleotide sequence, expression and transcriptional analysis of the Corynebacterium glutamicum gltA gene encoding citrate synthase. Microbiology 140:1817–1828
     [Google Scholar]
  21. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580
     [Google Scholar]
  22. Huson D. H., Richter D. C., Rausch C., Dezulian T., Franz M., Rupp R. 2007; Dendroscope – an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460
     [Google Scholar]
  23. Ikeda M., Nakagawa S. 2003; The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol 62:99–109
     [Google Scholar]
  24. Kalinowski J., Bathe B., Bartels D., Bischoff M., Bott M., Burkovski A., Dusch N., Eggeling L., Eikmanns B. J. other authors 2003; The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of l-aspartate-derived amino acids and vitamins. J Biotechnol 104:5–25
     [Google Scholar]
  25. Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K. F., Itoh M., Kawashima S., Katayama T., Araki M., Hirakawa M. 2006; From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354–D357
     [Google Scholar]
  26. Le Breton Y., Pichereau V., Sauvageot N., Auffray Y., Rince A. 2005; Maltose utilization in Enterococcus faecalis . J Appl Microbiol 98:806–813
     [Google Scholar]
  27. Levander F., Andersson U., Radström P. 2001; Physiological role of β -phophoglucomutase in Lactococcus lactis . Appl Environ Microbiol 67:4546–4553
     [Google Scholar]
  28. Liebl W. 2005; Corynebacterium taxonomy. In Handbook of Corynebacterium glutamicum pp 9–34 Edited by Eggeling L., Bott M. Boca Raton, FL: CRC Press;
     [Google Scholar]
  29. Lu M., Kleckner N. 1994; Molecular cloning and characterization of the pgm gene encoding phosphoglucomutase of Escherichia coli . J Bacteriol 176:5847–5851
     [Google Scholar]
  30. Martin S. A., Russell J. B. 1987; Transport and phosphorylation of disaccharides by the ruminal bacterium Streptococcus bovis . Appl Environ Microbiol 53:2388–2393
     [Google Scholar]
  31. Mesak L. R., Dahl M. K. 2000; Purification and enzymatic characterization of PgcM, a β -phosphoglucomutase and glucose-1-phosphate dismutase of Bacillus subtilis . Arch Microbiol 174:256–264
     [Google Scholar]
  32. Meyer D., Schneider-Fresenius C., Horlacher R., Peist R., Boos W. 1997; Molecular characterization of glucokinase from Escherichia coli K-12. J Bacteriol 179:1298–1306
     [Google Scholar]
  33. Monod J., Torriani A. M. 1950; De l'amylomaltase d' Escherichia coli . Ann Inst Pasteur ( Paris ) 78:65–77
     [Google Scholar]
  34. Nilsson U., Radström P. 2001; Genetic localization and regulation of the maltose phosphorylase gene, malP , in Lactococcus lactis . Microbiology 147:1565–1573
     [Google Scholar]
  35. Park S.-Y., Kim H.-K., Yoo S.-K., Oh T.-K., Lee J. K. 2000; Characterization of glk , a gene coding for glucose kinase of Corynebacterium glutamicum . FEMS Microbiol Lett 188:209–215
     [Google Scholar]
  36. Pugsley A. P., Dubreuil C. 1988; Molecular characterization of malQ , the structural gene for the Escherichia coli enzyme amylomaltase. Mol Microbiol 2:473–479
     [Google Scholar]
  37. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  38. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A. 1994; Small mobilizable multi-purpose 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
     [Google Scholar]
  39. Schönert S., Seitz S., Krafft H., Feuerbaum E.-A., Andernach I., Witz G., Dahl M. K. 2006; Maltose and maltodextrin utilization by Bacillus subtilis . J Bacteriol 188:3911–3922
     [Google Scholar]
  40. Schwartz M. 1967; Phenotypic expression and genetic localization of mutations affecting maltose metabolism in Escherichia coli K12. Ann Inst Pasteur (Paris) 112:673–698 in French
    [Google Scholar]
  41. Seibold G. M., Eikmanns B. J. 2007; The glgX gene product of Corynebacterium glutamicum is required for glycogen degradation and for fast adaptation to hyperosmotic stress. Microbiology 153:2212–2220
     [Google Scholar]
  42. Seibold G. M., Auchter M., Berens S., Kalinowski J., Eikmanns B. J. 2006; Utilization of soluble starch by a recombinant Corynebacterium glutamicum strain: growth and lysine production. J Biotechnol 124:381–391
     [Google Scholar]
  43. Seibold G. M., Dempf S., Schreiner J., Eikmanns B. J. 2007; Glycogen formation in Corynebacterium glutamicum and role of ADP-glucose pyrophosphorylase. Microbiology 153:1275–1285
     [Google Scholar]
  44. Skarlatos P., Dahl M. K. 1998; The glucose kinase of Bacillus subtilis . J Bacteriol 180:3222–3226
     [Google Scholar]
  45. Takaha T., Yanase M., Takata H., Okada S. 2001; Structure and properties of Thermus aquaticus α -glucan phosphorylase expressed in Escherichia coli . J Appl Glycosci 48:71–78
     [Google Scholar]
  46. Tauch A., Homann I., Mormann S., Rüberg S., Billault A., Bathe B., Brand S., Brockmann-Gretza O., Rückert C. other authors 2002; Strategy to sequence the genome of Corynebacterium glutamicum ATCC 13032: use of a cosmid and a bacterial artificial chromosome library. J Biotechnol 95:25–38
     [Google Scholar]
  47. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
     [Google Scholar]
  48. Thompson J., Pikis A., Ruvinov S. B., Henrissat B., Yamamoto H., Sekiguchi J. 1998; The gene glvA of Bacillus subtilis 168 encodes a metal-requiring, NAD(H)-dependent 6-phospho- α -glucosidase. J Biol Chem 273:27347–27356
     [Google Scholar]
  49. Tropis M., Meniche X., Wolf A., Gebhard H., Strelkow S., Chami M., Schomburg D., Krämer R., Morbach S., Daffé M. 2005; The crucial role of trehalose and structurally related oligosaccharides in the biosynthesis and transfer of mycolic acids in Corynebacterianeae. J Biol Chem 280:26573–26585
     [Google Scholar]
  50. Tzvetkov M., Klopprogge C., Zelder O., Liebl W. 2003; Genetic dissection of trehalose biosynthesis in Corynebacterium glutamicum : inactivation of trehalose production leads to impaired growth and an altered cell wall composition. Microbiology 149:1659–1673
     [Google Scholar]
  51. Watson K. A., McCleverty C., Geremia S., Cottaz S., Driguez H., Johnson L. N. 1999; Phosphorylase recognition and phosphorolysis of its oligosaccharide substrate: answers to a long outstanding question. EMBO J 18:4619–4632
     [Google Scholar]
  52. Weinhäusel A., Griessler R., Krebs A., Zipper P., Haltrich D., Kube K. D., Nidetzky B. 1997; α -1,4-d-Glucan phosphorylase of Gram-positive Corynebacterium callunae : isolation, biochemical properties and molecular shape of the enzyme from solution X-ray scattering. Biochem J 326:773–783
     [Google Scholar]
  53. Wolf A., Krämer R., Morbach S. 2003; Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC 13032 and their significance in response to osmotic stress. Mol Microbiol 49:1119–1134
     [Google Scholar]
  54. Woodruff P. J., Carlson B. L., Siridechadilok B., Pratt M. R., Senaratne R. H., Mougous J. D., Riley L. W., Williams S. J., Bertozzi C. R. 2004; Trehalose is required for growth of Mycobacterium smegmatis . J Biol Chem 279:28835–28843
     [Google Scholar]
  55. Xavier K. B., Peist R., Kossmann M., Boos W., Santos H. 1999; Maltose metabolism in the hyperthermophilic archaeon Thermococcus litoralis : purification and characterization of key enzymes. J Bacteriol 181:3358–3367
     [Google Scholar]
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Roles of maltodextrin and glycogen phosphorylases in maltose utilization and glycogen metabolism in Corynebacterium glutamicum
Microbiology 155, 347 (2009); https://doi.org/10.1099/mic.0.023614-0
/content/journal/micro/10.1099/mic.0.023614-0
/content/journal/micro/10.1099/mic.0.023614-0
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