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Glycogen with short average chain length enhances bacterial durability

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Abstract

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.

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References

  • 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 277:42164–42170

    Article  PubMed  CAS  Google Scholar 

  • Abdelakher M, Smith F (1951) The repeating unit of glycogen. J Am Chem Soc 73:994–996

    Article  CAS  Google Scholar 

  • 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 188:5266–5272

    Article  PubMed  CAS  Google Scholar 

  • 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 263:9271–9275

    PubMed  CAS  Google Scholar 

  • Ball SG, Morell MK (2003) From bacterial glycogen to starch: Understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54:207–233

    Article  PubMed  CAS  Google Scholar 

  • Ballicora MA, Iglesias AA, Preiss J (2003) ADP-glucose pyrophosphorylase, a regulatory enzyme for bacterial glycogen synthesis. Microbiol Mol Biol Rev 67:213–225

    Article  PubMed  CAS  Google Scholar 

  • Bender H (1979) Glycogen from Klebsiella pneumoniae M5 al and Escherichia coli K12. Appl Microbiol Biotechnol 8:279–287

    Article  CAS  Google Scholar 

  • Binderup K, Mikkelsen R, Preiss J (2000) Limited proteolysis of branching enzyme from Escherichia coli. Arch Biochem Biophys 377:366–371

    Article  PubMed  CAS  Google Scholar 

  • Binderup M, Mikkelsen R, Preiss J (2002) Truncation of the amino terminus of branching enzyme changes its chain transfer pattern. Arch Biochem Biophys 397:279–285

    Article  PubMed  CAS  Google Scholar 

  • Boeck B, Schinzel R (1998) Growth dependence of alpha-glucan phosphorylase activity in Thermus thermophilus. Res Microbiol 149:171–176

    Article  PubMed  CAS  Google Scholar 

  • Boor KJ (2006) Bacterial stress responses: what doesn’t kill them can make them stronger. Plos Biol 4:18–20

    Article  CAS  Google Scholar 

  • Boylen CW, Mulks MH (1978) Survival of Coryneform bacteria during periods of prolonged nutrient starvation. J Gen Microbiol 105:323–334

    CAS  Google Scholar 

  • Brammer GL, Rougvie MA, French D (1972) Distribution of alpha-amylase-resistant regions in the glycogen molecule. Carbohydr Res 24:343–354

    Article  PubMed  CAS  Google Scholar 

  • Builder JE, Walker GJ (1970) Metabolism of the reserve polysaccharide of Streptococcus mitis. Properties of glycogen synthetase. Carbohydr Res 14:35–51

    Article  CAS  Google Scholar 

  • 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 23:3196–3205

    Article  PubMed  CAS  Google Scholar 

  • Chao L, Bowen CC (1971) Purification and properties of glycogen isolated from a blue-green alga, Nostoc muscorum. J Bacteriol 105:331–338

    PubMed  CAS  Google Scholar 

  • 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 67:1–12

    Article  PubMed  CAS  Google Scholar 

  • D’Hulst C, Merida A (2010) The priming of storage glucan synthesis from bacteria to plants: current knowledge and new developments. New Phytol 188:13–21

    Article  PubMed  Google Scholar 

  • 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 187:1465–1473

    Article  PubMed  CAS  Google Scholar 

  • 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 418:34–38

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Erlander SR, French D (1958) Acid hydrolysis and molecular weights of various corn amylopectin and glycogen. J Polym Sci 32:291–316

    Article  CAS  Google Scholar 

  • 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 581:4417–4422

    Article  PubMed  CAS  Google Scholar 

  • 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 581:2947–2953

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein DB, Brassell SC, Pratt LM (2010) Microbial biosynthesis of wax esters during desiccation: Adaptation for colonization of the earliest terrestrial environments? Geology 38:247–250

    Article  CAS  Google Scholar 

  • French D (1964) Structure of glycogen and its amylolytic degradation. In: Whelan WJ (ed) Control of Glycogen Metabolism. Churchill, London, pp 7–28

    Google Scholar 

  • Gallagher PK, Brown ME, Kemp RB (1998) Handbook of thermal analysis and calorimetry. Elsevier, Amsterdam

    Google Scholar 

  • 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 92:964–967

    Article  PubMed  CAS  Google Scholar 

  • 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 12:101–104

    Article  PubMed  Google Scholar 

  • Gurr MI, Harwood JL, Frayn KN (2002) Lipid biochemistry, 5th edn. Blackwell, Oxford

    Book  Google Scholar 

  • Hara F, Akazawa T, Kojima K (1973) Glycogen biosynthesis in Chromatium strain D: I. characterization of glycogen. Plant Cell Physiol 14:737–745

    CAS  Google Scholar 

  • Henrissat B, Deleury E, Coutinho PM (2002) Glycogen metabolism loss: a common marker of parasitic behaviour in bacteria? Trends Genet 18:437–440

    Article  PubMed  CAS  Google Scholar 

  • Inglis TJJ, Sagripanti JL (2006) Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl Environ Microbiol 72:6865–6875

    Article  PubMed  CAS  Google Scholar 

  • Ishige T, Tani A, Sakai YR, Kato N (2003) Wax ester production by bacteria. Curr Opin Microbiol 6:244–250

    Article  PubMed  CAS  Google Scholar 

  • 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 527–535

    Chapter  Google Scholar 

  • Kamio Y, Terawaki Y, Nakajima T, Matsuda K (1981) Structure of glycogen produced by Selenomonas ruminantium. Agric Biol Chem 45:209–216

    Article  CAS  Google Scholar 

  • Kent PW, Stacey M (1949) Studies in the glycogen of M. Tuberculosis (human strain). Biochim Biophys Acta 3:641–647

    Article  CAS  Google Scholar 

  • Kim BH, Gadd GM (2008) Bacterial physiology and metabolism. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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 357:1507–1514

    Article  PubMed  CAS  Google Scholar 

  • Konig H, Skorko R, Zillig W, Reiter WD (1982) Glycogen in thermoacidophilic archaebacteria of the genera Sulfolobus, Thermoproteus, Desulfurococcus and Thermococcus. Arch Microbiol 132:297–303

    Article  Google Scholar 

  • Kornacker MG, Pugsley AP (1990) Molecular characterization of pulA and its product, pullulanase, a secreted enzyme of Klebsiella pneumoniae UNF5023. Mol Microbiol 4:73–85

    Article  PubMed  CAS  Google Scholar 

  • Kornberg A, Rao NN, Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68:89–125

    Article  PubMed  CAS  Google Scholar 

  • Kozlov G, Elias D, Cygler M, Gehring K (2004) Structure of GlgS from Escherichia coli suggests a role in protein-protein interactions. BMC Biol 2:10

    Article  PubMed  Google Scholar 

  • Laidig KE (1991) Energetics of hydrocarbon branching. J Phys Chem 95:7709–7713

    Article  CAS  Google Scholar 

  • Lappinscott HM, Cusack F, Macleod A, Costerton JW (1988) Starvation and nutrient resuscitation of Klebsiella pneumoniae isolated from oil well waters. J Appl Bacteriol 64:541–549

    CAS  Google Scholar 

  • 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 82:279–293

    PubMed  CAS  Google Scholar 

  • 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–D478

    Article  PubMed  CAS  Google Scholar 

  • Lopez NI, Ruiz JA, Mendez BS (1998) Survival of poly-3-hydroxybutyrate-producing bacteria in soil microcosms. World J Microbiol Biotechnol 14:681–684

    Article  CAS  Google Scholar 

  • Lou J, Dawson KA, Strobel HJ (1997) Glycogen formation by the ruminal bacterium Prevotella ruminicola. Appl Environ Microbiol 63:1483–1488

    PubMed  CAS  Google Scholar 

  • Manners DJ (1957) The molecular structure of glycogens. Adv Carbohydr Chem Biochem 12:261–298

    CAS  Google Scholar 

  • Manners DJ (1991) Recent Developments in our understanding of glycogen structure. Carbohydr Polym 16:37–82

    Article  CAS  Google Scholar 

  • 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 179:7784–7789

    PubMed  CAS  Google Scholar 

  • Melendez R, Melendez-Hevia E, Canela EI (1999) The fractal structure of glycogen: A clever solution to optimize cell metabolism. Biophys J 77:1327–1332

    Article  PubMed  CAS  Google Scholar 

  • Meléndez-Hevia E, Waddell TG, Shelton ED (1993) Optimization of molecular design in the evolution of metabolism: the glycogen molecule. Biochem J 295:477–483

    PubMed  Google Scholar 

  • 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 433:107–117

    Article  PubMed  Google Scholar 

  • Moran NA (2002) Microbial minimalism: Genome reduction in bacterial pathogens. Cell 108:583–586

    Article  PubMed  CAS  Google Scholar 

  • 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 581:4423–4429

    Article  PubMed  CAS  Google Scholar 

  • 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 9:141–148

    Article  PubMed  CAS  Google Scholar 

  • 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–E951

    Article  PubMed  CAS  Google Scholar 

  • 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 75:1355–1362

    Article  PubMed  CAS  Google Scholar 

  • 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 44:792–800

    Article  PubMed  CAS  Google Scholar 

  • 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 46:36–42

    Article  PubMed  CAS  Google Scholar 

  • Park JT, Yu LP, Rollings JE (1988) Substrate structural effects on enzymatic depolymerization of amylose, amylopectin, and glycogen. Ann N Y Acad Sci 542:53–60

    Article  CAS  Google Scholar 

  • Preiss J (2009) Glycogen Biosynthesis. In: Schaechter M (ed) Encyclopedia of Microbiology, 3rd edn. Elsevier, Oxford, pp 145–158

    Chapter  Google Scholar 

  • Raha M, Kawagishi I, Muller V, Kihara M, Macnab RM (1992) Escherichia coli produces a cytoplasmic alpha-amylase, AmyA. J Bacteriol 174:6644–6652

    PubMed  CAS  Google Scholar 

  • Sakharkar KR, Chow VT (2005) Strategies for genome reduction in microbial genomes. Genome Inform 16:69–75

    PubMed  CAS  Google Scholar 

  • Scherp HW (1955) Neisseria and Neisserial infections. Annu Rev Microbiol 9:319–334

    Article  PubMed  CAS  Google Scholar 

  • 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 74:159–174

    Article  PubMed  CAS  Google Scholar 

  • Strange RE (1968) Bacterial glycogen and survival. Nature 220:606–607

    Article  PubMed  CAS  Google Scholar 

  • Strange RE, Ness AG, Dark FA (1961) Survival of stationary phase Aerobacter aerogenes stored in aqueous suspension. J Gen Microbiol 25:61–67

    CAS  Google Scholar 

  • 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 11:1094–1100

    Article  PubMed  CAS  Google Scholar 

  • Swanson MA, Cori CF (1948) Studies on the structure of polysaccharides: acid hydrolysis of starch-like polysaccharides. J Biol Chem 172:797–804

    PubMed  CAS  Google Scholar 

  • 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 59:290–294

    Google Scholar 

  • Takahata Y, Hoaki T, Maruyama T (2001) Starvation survivability of Thermococcus strains isolated from Japanese oil reservoirs. Arch Microbiol 176:264–270

    Article  PubMed  CAS  Google Scholar 

  • 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 179:4689–4698

    PubMed  CAS  Google Scholar 

  • Takata H, Takaha T, Okada S, Takagi M, Imanaka T (1998) Purification and characterization of alpha-glucan phosphorylase from Bacillus stearothermophilus. J Ferment Bioeng 85:156–161

    Article  CAS  Google Scholar 

  • Tewari YB, Goldberg RN (1989) Thermodynamics of hydrolysis of disaccharides. Cellobiose, gentiobiose, isomaltose, and maltose. J Biol Chem 264:3966–3971

    PubMed  CAS  Google Scholar 

  • Tsintzas K, Williams C (1998) Human muscle glycogen metabolism during exercise. Effect of carbohydrate supplementation. Sports Med 25:7–23

    Article  PubMed  CAS  Google Scholar 

  • Wallace RJ (1980) Cytoplasmic reserve polysaccharide of Selenomonas ruminantium. Appl Environ Microbiol 39:630–634

    PubMed  CAS  Google Scholar 

  • Waltermann M, Steinbuchel A (2005) Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J Bacteriol 187:3607–3619

    Article  PubMed  Google Scholar 

  • Walther BA, Ewald PW (2004) Pathogen survival in the external environment and the evolution of virulence. Biol Rev Camb Philos Soc 79:849–869

    Article  PubMed  Google Scholar 

  • 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 39:295–302

    Article  PubMed  CAS  Google Scholar 

  • Whyte JN, Strasdin GA (1972) An intracellular alpha-D-glucan from Clostridium botulinum, type E. Carbohydr Res 25:435–441

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson JF (1963) Carbon and energy storage in bacteria. J Gen Microbiol 32:171–176

    PubMed  CAS  Google Scholar 

  • 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 34:952–958

    PubMed  CAS  Google Scholar 

  • Wolfrom ML, Lassettre EN, Oneill AN (1951) Degradation of glycogen to isomaltose. J Am Chem Soc 73:595–599

    Article  CAS  Google Scholar 

  • Yang XR, Miller MA, Yang R, Evans DF, Edstrom RD (1990) Scanning tunneling microscopic images show a laminated structure for glycogen molecules. FASEB J 4:3140–3143

    PubMed  CAS  Google Scholar 

  • 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 40:498–504

    Article  PubMed  CAS  Google Scholar 

  • Young FG (1957) Claude Bernard and the discovery of glycogen: a century of retrospect. Br Med J 1:1431–1437

    Article  PubMed  CAS  Google Scholar 

  • Zevenhuizen LP (1992) Levels of trehalose and glycogen in Arthrobacter globiformis under conditions of nutrient starvation and osmotic stress. Antonie Leeuwenhoek 61:61–68

    Article  PubMed  CAS  Google Scholar 

  • Zevenhuizen LP, Ebbink AG (1974) Interrelations between glycogen, poly-beta-hydroxybutyric acid and lipids during accumulation and subsequent utilization in a Pseudomonas. Antonie Leeuwenhoek 40:103–120

    Article  PubMed  CAS  Google Scholar 

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  1. School of Biomedical, Biomolecular and Chemical Sciences, The University of Western Australia (M502), 35 Stirling Highway, Perth, WA, 6009, Australia

    Liang Wang

  2. School of Biomedical, Biomolecular and Chemical Sciences, The University of Western Australia (M310), 35 Stirling Highway, Perth, WA, 6009, Australia

    Michael J. Wise

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  1. Liang Wang
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Wang, L., Wise, M.J. Glycogen with short average chain length enhances bacterial durability. Naturwissenschaften 98, 719 (2011). https://doi.org/10.1007/s00114-011-0832-x

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