, 98:719 | Cite as

Glycogen with short average chain length enhances bacterial durability

  • Liang Wang
  • Michael J. WiseEmail author


Glycogen is conventionally viewed as an energy reserve that can be rapidly mobilized for ATP production in higher organisms. However, several studies have noted that glycogen with short average chain length in some bacteria is degraded very slowly. In addition, slow utilization of glycogen is correlated with bacterial viability, that is, the slower the glycogen breakdown rate, the longer the bacterial survival time in the external environment under starvation conditions. We call that a durable energy storage mechanism (DESM). In this review, evidence from microbiology, biochemistry, and molecular biology will be assembled to support the hypothesis of glycogen as a durable energy storage compound. One method for testing the DESM hypothesis is proposed.


Glycogen Average chain length Hidden Markov Model Glycosidic linkage Durability 

Supplementary material

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ESM 1 (XLS 1787 kb)


  1. Abad MC, Binderup K, Rios-Steiner J, Arni RK, Preiss J, Geiger JH (2002) The X-ray crystallographic structure of Escherichia coli branching enzyme. J Biol Chem 277:42164–42170PubMedCrossRefGoogle Scholar
  2. Abdelakher M, Smith F (1951) The repeating unit of glycogen. J Am Chem Soc 73:994–996CrossRefGoogle Scholar
  3. Alonso-Casajus N, Dauvillee D, Viale AM, Munoz FJ, Baroja-Fernandez E, Moran-Zorzano MT, Eydallin G, Ball S, Pozueta-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 188:5266–5272PubMedCrossRefGoogle Scholar
  4. Amemura A, Chakraborty R, Fujita M, Noumi T, Futai M (1988) Cloning and nucleotide sequence of the isoamylase gene from Pseudomonas amyloderamosa SB-15. J Biol Chem 263:9271–9275PubMedGoogle Scholar
  5. Ball SG, Morell MK (2003) From bacterial glycogen to starch: Understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54:207–233PubMedCrossRefGoogle Scholar
  6. Ballicora MA, Iglesias AA, Preiss J (2003) ADP-glucose pyrophosphorylase, a regulatory enzyme for bacterial glycogen synthesis. Microbiol Mol Biol Rev 67:213–225PubMedCrossRefGoogle Scholar
  7. Bender H (1979) Glycogen from Klebsiella pneumoniae M5 al and Escherichia coli K12. Appl Microbiol Biotechnol 8:279–287CrossRefGoogle Scholar
  8. Binderup K, Mikkelsen R, Preiss J (2000) Limited proteolysis of branching enzyme from Escherichia coli. Arch Biochem Biophys 377:366–371PubMedCrossRefGoogle Scholar
  9. Binderup M, Mikkelsen R, Preiss J (2002) Truncation of the amino terminus of branching enzyme changes its chain transfer pattern. Arch Biochem Biophys 397:279–285PubMedCrossRefGoogle Scholar
  10. Boeck B, Schinzel R (1998) Growth dependence of alpha-glucan phosphorylase activity in Thermus thermophilus. Res Microbiol 149:171–176PubMedCrossRefGoogle Scholar
  11. Boor KJ (2006) Bacterial stress responses: what doesn’t kill them can make them stronger. Plos Biol 4:18–20CrossRefGoogle Scholar
  12. Boylen CW, Mulks MH (1978) Survival of Coryneform bacteria during periods of prolonged nutrient starvation. J Gen Microbiol 105:323–334Google Scholar
  13. Brammer GL, Rougvie MA, French D (1972) Distribution of alpha-amylase-resistant regions in the glycogen molecule. Carbohydr Res 24:343–354PubMedCrossRefGoogle Scholar
  14. Builder JE, Walker GJ (1970) Metabolism of the reserve polysaccharide of Streptococcus mitis. Properties of glycogen synthetase. Carbohydr Res 14:35–51CrossRefGoogle Scholar
  15. Buschiazzo A, Ugalde JE, Guerin ME, Shepard W, Ugalde RA, Alzari PM (2004) Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J 23:3196–3205PubMedCrossRefGoogle Scholar
  16. Chao L, Bowen CC (1971) Purification and properties of glycogen isolated from a blue-green alga, Nostoc muscorum. J Bacteriol 105:331–338PubMedGoogle Scholar
  17. Cho KM, Lim WJ, Math RK, Islam SMA, Hong SJ, Kim H, Yun HD (2008) Comparative analysis of the glg operons of Pectobacterium chrysanthemi PY35 and other prokaryotes. J Mol Evol 67:1–12PubMedCrossRefGoogle Scholar
  18. D’Hulst C, Merida A (2010) The priming of storage glucan synthesis from bacteria to plants: current knowledge and new developments. New Phytol 188:13–21PubMedCrossRefGoogle Scholar
  19. Dauvillee D, Kinderf IS, Li ZY, Kosar-Hashemi B, Samuel MS, Rampling L, Ball S, Morell MK (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187:1465–1473PubMedCrossRefGoogle Scholar
  20. Devillers CH, Piper ME, Ballicora MA, Preiss J (2003) Characterization of the branching patterns of glycogen branching enzyme truncated on the N-terminus. Arch Biochem Biophys 418:34–38PubMedCrossRefGoogle Scholar
  21. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763PubMedCrossRefGoogle Scholar
  22. Erlander SR, French D (1958) Acid hydrolysis and molecular weights of various corn amylopectin and glycogen. J Polym Sci 32:291–316CrossRefGoogle Scholar
  23. Eydallin G, Moran-Zorzano MT, Munoz FJ, Baroja-Fernandez E, Montero M, Alonso-Casajus N, Viale AM, Pozueta-Romero J (2007a) An Escherichia coli mutant producing a truncated inactive form of GlgC synthesizes glycogen: Further evidences for the occurrence of various important sources of ADPglucose in enterobacteria. FEBS Lett 581:4417–4422PubMedCrossRefGoogle Scholar
  24. Eydallin G, Viale AM, Moran-Zorzano MT, Munoz FJ, Montero M, Baroja-Fernandez E, Pozueta-Romero J (2007b) Genome-wide screening of genes affecting glycogen metabolism in Escherichia coli K-12. FEBS Lett 581:2947–2953PubMedCrossRefGoogle Scholar
  25. Finkelstein DB, Brassell SC, Pratt LM (2010) Microbial biosynthesis of wax esters during desiccation: Adaptation for colonization of the earliest terrestrial environments? Geology 38:247–250CrossRefGoogle Scholar
  26. French D (1964) Structure of glycogen and its amylolytic degradation. In: Whelan WJ (ed) Control of Glycogen Metabolism. Churchill, London, pp 7–28Google Scholar
  27. Gallagher PK, Brown ME, Kemp RB (1998) Handbook of thermal analysis and calorimetry. Elsevier, AmsterdamGoogle Scholar
  28. Guan H, Kuriki T, Sivak M, Preiss J (1995) Maize branching enzyme catalyzes synthesis of glycogen-like polysaccharide in glgB-deficient Escherichia coli. Proc Natl Acad Sci USA 92:964–967PubMedCrossRefGoogle Scholar
  29. Gunja-Smith Z, Marshall JJ, Mercier C, Smith EE, Whelan WJ (1970) A revision of the Meyer-Bernfeld model of glycogen and amylopectin. FEBS Lett 12:101–104PubMedCrossRefGoogle Scholar
  30. Gurr MI, Harwood JL, Frayn KN (2002) Lipid biochemistry, 5th edn. Blackwell, OxfordCrossRefGoogle Scholar
  31. Hara F, Akazawa T, Kojima K (1973) Glycogen biosynthesis in Chromatium strain D: I. characterization of glycogen. Plant Cell Physiol 14:737–745Google Scholar
  32. Henrissat B, Deleury E, Coutinho PM (2002) Glycogen metabolism loss: a common marker of parasitic behaviour in bacteria? Trends Genet 18:437–440PubMedCrossRefGoogle Scholar
  33. Inglis TJJ, Sagripanti JL (2006) Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl Environ Microbiol 72:6865–6875PubMedCrossRefGoogle Scholar
  34. Ishige T, Tani A, Sakai YR, Kato N (2003) Wax ester production by bacteria. Curr Opin Microbiol 6:244–250PubMedCrossRefGoogle Scholar
  35. Kalscheuer R (2010) Genetics of wax ester and triacylglycerol biosynthesis in bacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, 1st edn. Springer, New York, pp 527–535CrossRefGoogle Scholar
  36. Kamio Y, Terawaki Y, Nakajima T, Matsuda K (1981) Structure of glycogen produced by Selenomonas ruminantium. Agric Biol Chem 45:209–216CrossRefGoogle Scholar
  37. Kent PW, Stacey M (1949) Studies in the glycogen of M. Tuberculosis (human strain). Biochim Biophys Acta 3:641–647CrossRefGoogle Scholar
  38. Kim BH, Gadd GM (2008) Bacterial physiology and metabolism. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. Kollberg G, Tulinius M, Gilljam T, Ostman-Smith I, Forsander G, Jotorp P, Oldfors A, Holme E (2007) Cardiomyopathy and exercise intolerance in muscle glycogen storage disease 0. N Engl J Med 357:1507–1514PubMedCrossRefGoogle Scholar
  40. Konig H, Skorko R, Zillig W, Reiter WD (1982) Glycogen in thermoacidophilic archaebacteria of the genera Sulfolobus, Thermoproteus, Desulfurococcus and Thermococcus. Arch Microbiol 132:297–303CrossRefGoogle Scholar
  41. Kornacker MG, Pugsley AP (1990) Molecular characterization of pulA and its product, pullulanase, a secreted enzyme of Klebsiella pneumoniae UNF5023. Mol Microbiol 4:73–85PubMedCrossRefGoogle Scholar
  42. Kornberg A, Rao NN, Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68:89–125PubMedCrossRefGoogle Scholar
  43. Kozlov G, Elias D, Cygler M, Gehring K (2004) Structure of GlgS from Escherichia coli suggests a role in protein-protein interactions. BMC Biol 2:10PubMedCrossRefGoogle Scholar
  44. Laidig KE (1991) Energetics of hydrocarbon branching. J Phys Chem 95:7709–7713CrossRefGoogle Scholar
  45. Lappinscott HM, Cusack F, Macleod A, Costerton JW (1988) Starvation and nutrient resuscitation of Klebsiella pneumoniae isolated from oil well waters. J Appl Bacteriol 64:541–549Google Scholar
  46. Lares C, Frixon C, Creuzet-Sigal N, Thomas P (1974) Characterization and ultrastructure of mutants of Escherichia coli deficient in alpha-1,4-glucan-alpha-1,4-glucan 6-glycosytransferase (branching enzyme). J Gen Microbiol 82:279–293PubMedGoogle Scholar
  47. Lima T, Auchincloss AH, Coudert E, Keller G, Michoud K, Rivoire C, Bulliard V, de Castro E, Lachaize C, Baratin D, Phan I, Bougueleret L, Bairoch A (2009) HAMAP: a database of completely sequenced microbial proteome sets and manually curated microbial protein families in UniProtKB/Swiss-Prot. Nucleic Acids Res 37:D471–D478PubMedCrossRefGoogle Scholar
  48. Lopez NI, Ruiz JA, Mendez BS (1998) Survival of poly-3-hydroxybutyrate-producing bacteria in soil microcosms. World J Microbiol Biotechnol 14:681–684CrossRefGoogle Scholar
  49. Lou J, Dawson KA, Strobel HJ (1997) Glycogen formation by the ruminal bacterium Prevotella ruminicola. Appl Environ Microbiol 63:1483–1488PubMedGoogle Scholar
  50. Manners DJ (1957) The molecular structure of glycogens. Adv Carbohydr Chem Biochem 12:261–298Google Scholar
  51. Manners DJ (1991) Recent Developments in our understanding of glycogen structure. Carbohydr Polym 16:37–82CrossRefGoogle Scholar
  52. Martin MC, Schneider D, Bruton CJ, Chater KF, Hardisson C (1997) A glgC gene essential only for the first of two spatially distinct phases of glycogen synthesis in Streptomyces coelicolor A3(2). J Bacteriol 179:7784–7789PubMedGoogle Scholar
  53. Melendez R, Melendez-Hevia E, Canela EI (1999) The fractal structure of glycogen: A clever solution to optimize cell metabolism. Biophys J 77:1327–1332PubMedCrossRefGoogle Scholar
  54. Meléndez-Hevia E, Waddell TG, Shelton ED (1993) Optimization of molecular design in the evolution of metabolism: the glycogen molecule. Biochem J 295:477–483PubMedGoogle Scholar
  55. Montero M, Almagro G, Eydallin G, Viale AM, Muñoz FJ, Bahaji A, Li J, Rahimpour M, Baroja-Fernández E, Pozueta-Romero J (2010) Escherichia coli glycogen genes are organized in a single glgBXCAP transcriptional unit possessing an alternative suboperonic promoter within glgC that directs glgAP expression. Biochem J 433:107–117PubMedCrossRefGoogle Scholar
  56. Moran NA (2002) Microbial minimalism: Genome reduction in bacterial pathogens. Cell 108:583–586PubMedCrossRefGoogle Scholar
  57. Moran-Zorzano MT, Alonso-Casajus N, Munoz FJ, Viale AM, Baroja-Fernandez E, Eydallin G, Pozueta-Romero J (2007) Occurrence of more than one important source of ADPglucose linked to glycogen biosynthesis in Escherichia coli and Salmonella. FEBS Lett 581:4423–4429PubMedCrossRefGoogle Scholar
  58. Norrman J, Wober G, Cantino EC (1975) Variation in average unit chain-length of glycogen in relation to developmental stage in Blastocladiella Emersonii. Mol Cell Biochem 9:141–148PubMedCrossRefGoogle Scholar
  59. Oz G, Seaquist ER, Kumar A, Criego AB, Benedict LE, Rao JP, Henry PG, Van De Moortele PF, Gruetter R (2007) Human brain glycogen content and metabolism: implications on its role in brain energy metabolism. Am J Physiol Endocrinol Metab 292:E946–E951PubMedCrossRefGoogle Scholar
  60. Palomo M, Kralj S, van der Maarel MJEC, Dijkhuizen L (2009) The unique branching patterns of Deinococcus glycogen branching enzymes are determined by their N-terminal domains. Appl Environ Microbiol 75:1355–1362PubMedCrossRefGoogle Scholar
  61. Park JT, Rollings JE (1994) Effects of substrate branching characteristics on kinetics of enzymatic depolymerizaion of mixed linear and branched polysaccharides: I. amylose/amylopectin alpha-amylolysis. Biotechnol Bioeng 44:792–800PubMedCrossRefGoogle Scholar
  62. Park JT, Rollings JE (1995) Effects of substrate branching characteristics on kinetics of enzymatic depolymerization of mixed linear and branched polysaccharides: II. amylose/glycogen alpha-amylolysis. Biotechnol Bioeng 46:36–42PubMedCrossRefGoogle Scholar
  63. Park JT, Yu LP, Rollings JE (1988) Substrate structural effects on enzymatic depolymerization of amylose, amylopectin, and glycogen. Ann N Y Acad Sci 542:53–60CrossRefGoogle Scholar
  64. Preiss J (2009) Glycogen Biosynthesis. In: Schaechter M (ed) Encyclopedia of Microbiology, 3rd edn. Elsevier, Oxford, pp 145–158CrossRefGoogle Scholar
  65. Raha M, Kawagishi I, Muller V, Kihara M, Macnab RM (1992) Escherichia coli produces a cytoplasmic alpha-amylase, AmyA. J Bacteriol 174:6644–6652PubMedGoogle Scholar
  66. Sakharkar KR, Chow VT (2005) Strategies for genome reduction in microbial genomes. Genome Inform 16:69–75PubMedGoogle Scholar
  67. Scherp HW (1955) Neisseria and Neisserial infections. Annu Rev Microbiol 9:319–334PubMedCrossRefGoogle Scholar
  68. Shelburne SA, Keith DB, Davenport MT, Beres SB, Carroll RK, Musser JM (2009) Contribution of AmyA, an extracellular alpha-glucan degrading enzyme, to group A streptococcal host-pathogen interaction. Mol Microbiol 74:159–174PubMedCrossRefGoogle Scholar
  69. Strange RE (1968) Bacterial glycogen and survival. Nature 220:606–607PubMedCrossRefGoogle Scholar
  70. Strange RE, Ness AG, Dark FA (1961) Survival of stationary phase Aerobacter aerogenes stored in aqueous suspension. J Gen Microbiol 25:61–67Google Scholar
  71. Sullivan MA, Vilaplana F, Cave RA, Stapleton D, Gray-Weale AA, Gilbert RG (2010) Nature of alpha and beta particles in glycogen using molecular size distributions. Biomacromolecules 11:1094–1100PubMedCrossRefGoogle Scholar
  72. Swanson MA, Cori CF (1948) Studies on the structure of polysaccharides: acid hydrolysis of starch-like polysaccharides. J Biol Chem 172:797–804PubMedGoogle Scholar
  73. Takahash K, Ono S (1966) Calorimetric studies on hydrolysis of glucosides. IV. calorimetric determination of alpha-1,4 glucosidic linkage content in some starches and glycogens. J Biochem 59:290–294Google Scholar
  74. Takahata Y, Hoaki T, Maruyama T (2001) Starvation survivability of Thermococcus strains isolated from Japanese oil reservoirs. Arch Microbiol 176:264–270PubMedCrossRefGoogle Scholar
  75. Takata H, Takaha T, Okada S, Takagi M, Imanaka T (1997) Characterization of a gene cluster for glycogen biosynthesis and a heterotetrameric ADP-glucose pyrophosphorylase from Bacillus stearothermophilus. J Bacteriol 179:4689–4698PubMedGoogle Scholar
  76. Takata H, Takaha T, Okada S, Takagi M, Imanaka T (1998) Purification and characterization of alpha-glucan phosphorylase from Bacillus stearothermophilus. J Ferment Bioeng 85:156–161CrossRefGoogle Scholar
  77. Tewari YB, Goldberg RN (1989) Thermodynamics of hydrolysis of disaccharides. Cellobiose, gentiobiose, isomaltose, and maltose. J Biol Chem 264:3966–3971PubMedGoogle Scholar
  78. Tsintzas K, Williams C (1998) Human muscle glycogen metabolism during exercise. Effect of carbohydrate supplementation. Sports Med 25:7–23PubMedCrossRefGoogle Scholar
  79. Wallace RJ (1980) Cytoplasmic reserve polysaccharide of Selenomonas ruminantium. Appl Environ Microbiol 39:630–634PubMedGoogle Scholar
  80. Waltermann M, Steinbuchel A (2005) Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J Bacteriol 187:3607–3619PubMedCrossRefGoogle Scholar
  81. Walther BA, Ewald PW (2004) Pathogen survival in the external environment and the evolution of virulence. Biol Rev Camb Philos Soc 79:849–869PubMedCrossRefGoogle Scholar
  82. Weber M, Wober G (1975) The fine structure of the branched alpha-D-glucan from the blue-green alga Anacystis nidulans: comparison with other bacterial glycogens and phytoglycogen. Carbohydr Res 39:295–302PubMedCrossRefGoogle Scholar
  83. Whyte JN, Strasdin GA (1972) An intracellular alpha-D-glucan from Clostridium botulinum, type E. Carbohydr Res 25:435–441PubMedCrossRefGoogle Scholar
  84. Wilkinson JF (1963) Carbon and energy storage in bacteria. J Gen Microbiol 32:171–176PubMedGoogle Scholar
  85. Wilson WA, Roach PJ, Montero M, Baroja-Fernandez E, Munoz FJ, Eydallin G, Viale AM, Pozueta-Romero J (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34:952–958PubMedGoogle Scholar
  86. Wolfrom ML, Lassettre EN, Oneill AN (1951) Degradation of glycogen to isomaltose. J Am Chem Soc 73:595–599CrossRefGoogle Scholar
  87. Yang XR, Miller MA, Yang R, Evans DF, Edstrom RD (1990) Scanning tunneling microscopic images show a laminated structure for glycogen molecules. FASEB J 4:3140–3143PubMedGoogle Scholar
  88. Yoo SH, Keppel C, Spalding M, Jane JL (2007) Effects of growth condition on the structure of glycogen produced in cyanobacterium Synechocystis sp PCC6803. Int J Biol Macromol 40:498–504PubMedCrossRefGoogle Scholar
  89. Young FG (1957) Claude Bernard and the discovery of glycogen: a century of retrospect. Br Med J 1:1431–1437PubMedCrossRefGoogle Scholar
  90. Zevenhuizen LP (1992) Levels of trehalose and glycogen in Arthrobacter globiformis under conditions of nutrient starvation and osmotic stress. Antonie Leeuwenhoek 61:61–68PubMedCrossRefGoogle Scholar
  91. Zevenhuizen LP, Ebbink AG (1974) Interrelations between glycogen, poly-beta-hydroxybutyric acid and lipids during accumulation and subsequent utilization in a Pseudomonas. Antonie Leeuwenhoek 40:103–120PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.School of Biomedical, Biomolecular and Chemical SciencesThe University of Western Australia (M502)PerthAustralia
  2. 2.School of Biomedical, Biomolecular and Chemical SciencesThe University of Western Australia (M310)PerthAustralia

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