MetaCyc Pathway: starch degradation III
Inferred from experiment

Pathway diagram: starch degradation III

This view shows enzymes only for those organisms listed below, in the list of taxa known to possess the pathway. If an enzyme name is shown in bold, there is experimental evidence for this enzymatic activity.

Superclasses: Degradation/Utilization/AssimilationCarbohydrates DegradationPolysaccharides DegradationStarch Degradation
Degradation/Utilization/AssimilationPolymeric Compounds DegradationPolysaccharides DegradationStarch Degradation

Some taxa known to possess this pathway include : Archaeoglobus fulgidus 7324

Expected Taxonomic Range: Archaea

General Background

Many organisms including bacteria, fungi, metazoa, and plants can degrade glucose polymers derived from starch or glycogen (see pathways starch degradation II, starch degradation I, glycogen degradation I and glycogen degradation II). Some hyperthermophilic archaea have also been shown to produce starch-degrading enzymes, and pathways for the utilization of starch and its derivatives, such as a cyclodextrin, a maltodextrin, and maltose have been proposed. These hyperthermophilic archaea can utilize starch and its degradation products as primary carbon sources during anaerobic growth. Thermostable starch-degrading enzymes produced by hyperthermophpilic organisms are of industrial interest [Lee06b, Hashimoto01, Labes07, Labes01].

The hyperthermophilic, sulfate-reducing archaeon Archaeoglobus fulgidus 7324 has been shown to degrade starch via a unique pathway involving cyclodextrin intermediates (see a cyclodextrin) as described below in About This Pathway [Labes07, Labes01]. Cyclodextrins (cyclomaltodextrins) are cyclic oligosaccharides composed of α-1,4-linked glucose units. Early literature referred to them as Schardinger dextrins. Cyclodextrins corresponding to 6-12+ glucose units have been characterized (in [DePinto68]) (see α-cyclodextrin, β-cyclodextrin, γ-cyclodextrin). The physicochemical properties of cyclodextrins give them broad applications in the food, cosmetic and pharmaceutical industries (in [Hashimoto01]).

The hyperthermophilic archaeon Pyrococcus furiosus DSM 3638 was shown to degrade starch mainly via maltodextrins in a pathway involving an extracellular amylopullulanase, a transporter, an intracellular 4-α-glucanotransferase, and a maltodextrin phosphorylase. These enzymes produce β-D-glucopyranose and α-D-glucopyranose 1-phosphate that are converted to β-D-glucose 6-phosphate and degraded in pathway glycolysis V (Pyrococcus) ( [Lee06b] and in [Labes07]) (see pathway starch degradation V).

In the hyperthermophilic archaeon Thermococcus sp. B1001 evidence suggested a starch degradation pathway via formation of cyclodextrins from starch extracellularly by a cyclomaltodextrin glucanotransferase, transport of cyclodextrins into the cell, and their degradation by a cyclodextrinase to the end products maltose and α-D-glucopyranose ( [Hashimoto01] and in [Labes07]) (see pathway starch degradation IV).

Among bacteria Escherichia coli cannot utilize starch, but it can metabolize short, linear maltodextrins (see pathway glycogen degradation I). However the enterobacterium Klebsiella oxytoca M5al can utilize starch as a sole source of carbon and energy. Mutant analysis suggested that it metabolizes starch by two pathways. The first was a proposed maltose/maltodextrin pathway involving extracellular degradation of starch by pullulanase and the disproportionation activity of cyclodextrin glucanotransferase to form linear maltodextins. After transport into the cell they are degraded to β-D-glucopyranose and α-D-glucopyranose 1-phosphate by the products of malP, malQ and malZ. The second was a proposed cyclodextrin pathway involving extracellular conversion of starch to cyclodextrins (see a cyclodextrin) by cyclodextrin glucanotransferase, transport into the cell, linearization by cyclodextrinase (CymH) [Feederle96], and further catabolism as in the maltose/maltodextrin pathway [Fiedler96, Pajatsch98].

About This Pathway

Archaeoglobus fulgidus 7324 is a sulfate-reducing, hyperthermophilic archaeon that was shown to utilize starch and sulfate as sources of carbon and energy. Starch was incompletely oxidized to acetate and CO2 via a glycolysis pathway that was enzymatically similar to the glycolysis V (Pyrococcus) pathway shown in the pathway link. Sulfate was reduced to hydrogen sulfide (see pathway sulfate reduction IV (dissimilatory)). The enzymes in this proposed pathway have been characterized as shown here. In contrast, it was noted that another strain, Archaeoglobus fulgidus DSM 4304, does not contain sugar utilization genes and is therefore unable to utilize sugars [Labes07].

This pathway of starch degradation begins with the extracellular production of cyclodextrins (see above) from starch by the membrane-associated enzyme cyclodextrin glucanotransferase. Cyclodextrins are proposed to be taken into the cell by an as yet uncharacterized transport system. Inside the cell they are hydrolyzed to a maltodextrin (maltooligosaccharides) by cyclodextrinase. α-D-glucopyranose 1-phosphate is produced from a maltodextrin (maltooligosaccharides) by maltodextrin phosphorylase. α-D-glucopyranose 1-phosphate is converted by phosphoglucomutase to α-D-glucose 6-phosphate. This compound can enter glycolysis [Labes07], possibly after spontaneous or enzymatic conversion to its epimer β-D-glucose 6-phosphate. Whether the α, β, or both α and β epimers are used depends upon the anomeric specificity of the glycolytic enzyme involved.

Variants: starch degradation I, starch degradation II, starch degradation IV, starch degradation V

Created 18-Feb-2011 by Fulcher CA, SRI International


Ball03: Ball SG, Morell MK (2003). "From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule." Annu Rev Plant Biol 54;207-33. PMID: 14502990

Ball11: Ball S, Colleoni C, Cenci U, Raj JN, Tirtiaux C (2011). "The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis." J Exp Bot 62(6);1775-801. PMID: 21220783

Buleon98: Buleon A, Colonna P, Planchot V, Ball S (1998). "Starch granules: structure and biosynthesis." Int J Biol Macromol 23(2);85-112. PMID: 9730163

DePinto68: DePinto JA, Campbell LL (1968). "Purification and properties of the amylase of Bacillus macerans." Biochemistry 7(1);114-20. PMID: 5758537

Feederle96: Feederle R, Pajatsch M, Kremmer E, Bock A (1996). "Metabolism of cyclodextrins by Klebsiella oxytoca m5a1: purification and characterisation of a cytoplasmically located cyclodextrinase." Arch Microbiol 165(3);206-12. PMID: 8599539

Fiedler96: Fiedler G, Pajatsch M, Bock A (1996). "Genetics of a novel starch utilisation pathway present in Klebsiella oxytoca." J Mol Biol 256(2);279-91. PMID: 8594196

Hashimoto01: Hashimoto Y, Yamamoto T, Fujiwara S, Takagi M, Imanaka T (2001). "Extracellular synthesis, specific recognition, and intracellular degradation of cyclomaltodextrins by the hyperthermophilic archaeon Thermococcus sp. strain B1001." J Bacteriol 183(17);5050-7. PMID: 11489857

Labes01: Labes A, Schonheit P (2001). "Sugar utilization in the hyperthermophilic, sulfate-reducing archaeon Archaeoglobus fulgidus strain 7324: starch degradation to acetate and CO2 via a modified Embden-Meyerhof pathway and acetyl-CoA synthetase (ADP-forming)." Arch Microbiol 176(5);329-38. PMID: 11702074

Labes07: Labes A, Schonheit P (2007). "Unusual starch degradation pathway via cyclodextrins in the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus strain 7324." J Bacteriol 189(24);8901-13. PMID: 17921308

Lee06b: Lee HS, Shockley KR, Schut GJ, Conners SB, Montero CI, Johnson MR, Chou CJ, Bridger SL, Wigner N, Brehm SD, Jenney FE, Comfort DA, Kelly RM, Adams MW (2006). "Transcriptional and biochemical analysis of starch metabolism in the hyperthermophilic archaeon Pyrococcus furiosus." J Bacteriol 188(6);2115-25. PMID: 16513741

Pajatsch98: Pajatsch M, Gerhart M, Peist R, Horlacher R, Boos W, Bock A (1998). "The periplasmic cyclodextrin binding protein CymE from Klebsiella oxytoca and its role in maltodextrin and cyclodextrin transport." J Bacteriol 180(10);2630-5. PMID: 9573146

Shearer02: Shearer J, Graham TE (2002). "New perspectives on the storage and organization of muscle glycogen." Can J Appl Physiol 27(2);179-203. PMID: 12179957

Other References Related to Enzymes, Genes, Subpathways, and Substrates of this Pathway

Accorsi89: Accorsi A, Piatti E, Piacentini MP, Gini S, Fazi A (1989). "Isoenzymes of phosphoglucomutase from human red blood cells: isolation and kinetic properties." Prep Biochem 19(3);251-71. PMID: 2533352

Boles94: Boles E, Liebetrau W, Hofmann M, Zimmermann FK (1994). "A family of hexosephosphate mutases in Saccharomyces cerevisiae." Eur J Biochem 220(1);83-96. PMID: 8119301

Britton68: Britton HG, Clarke JB (1968). "The mechanism of the phosphoglucomutase reaction. Studies on rabbit muscle phosphoglucomutase with flux techniques." Biochem J 110(2);161-80. PMID: 5726186

Csutora05: Csutora P, Strassz A, Boldizsar F, Nemeth P, Sipos K, Aiello DP, Bedwell DM, Miseta A (2005). "Inhibition of phosphoglucomutase activity by lithium alters cellular calcium homeostasis and signaling in Saccharomyces cerevisiae." Am J Physiol Cell Physiol 289(1);C58-67. PMID: 15703203

Duckworth73: Duckworth HW, Barber BH, Sanwal BD (1973). "The interaction of phosphoglucomutase with nucleotide inhibitors." J Biol Chem 248(4);1431-5. PMID: 4568817

Fu95: Fu L, Bounelis P, Dey N, Browne BL, Marchase RB, Bedwell DM (1995). "The posttranslational modification of phosphoglucomutase is regulated by galactose induction and glucose repression in Saccharomyces cerevisiae." J Bacteriol 177(11);3087-94. PMID: 7768805

Hashimoto67: Hashimoto T, Joshi JC, Del Rio C, Handler P (1967). "Phosphoglucomutase. IV. Inactivation by beryllium ions." J Biol Chem 242(8);1671-9. PMID: 4960829

Joshi64: Joshi JG, Handler P (1964). "Phosphoglucomutase. I. Purification and properties of phosphoglucomutase from Escherichia coli." J Biol Chem 239;2741-51. PMID: 14216423

Kofler00: Kofler H, Hausler RE, Schulz B, Groner F, Flugge UI, Weber A (2000). "Molecular characterisation of a new mutant allele of the plastid phosphoglucomutase in Arabidopsis, and complementation of the mutant with the wild-type cDNA." Mol Gen Genet 263(6);978-86. PMID: 10954083

Latendresse13: Latendresse M. (2013). "Computing Gibbs Free Energy of Compounds and Reactions in MetaCyc."

Lazarevic05: Lazarevic V, Soldo B, Medico N, Pooley H, Bron S, Karamata D (2005). "Bacillus subtilis alpha-phosphoglucomutase is required for normal cell morphology and biofilm formation." Appl Environ Microbiol 71(1);39-45. PMID: 15640167

Masuda01: Masuda CA, Xavier MA, Mattos KA, Galina A, Montero-Lomeli M (2001). "Phosphoglucomutase is an in vivo lithium target in yeast." J Biol Chem 276(41);37794-801. PMID: 11500487

Mizanur08a: Mizanur RM, Griffin AK, Pohl NL (2008). "Recombinant production and biochemical characterization of a hyperthermostable alpha-glucan/maltodextrin phosphorylase from Pyrococcus furiosus." Archaea 2(3);169-76. PMID: 19054743

Najjar54: Najjar VA, Pullman ME (1954). "The occurrence of a group transfer involving enzyme (phosphoglucomutase) and substrate." Science 119(3097);631-4. PMID: 13156640

Parche06: Parche S, Beleut M, Rezzonico E, Jacobs D, Arigoni F, Titgemeyer F, Jankovic I (2006). "Lactose-over-glucose preference in Bifidobacterium longum NCC2705: glcP, encoding a glucose transporter, is subject to lactose repression." J Bacteriol 188(4);1260-5. PMID: 16452407

Periappuram00: Periappuram C, Steinhauer L, Barton DL, Taylor DC, Chatson B, Zou J (2000). "The plastidic phosphoglucomutase from Arabidopsis. A reversible enzyme reaction with an important role in metabolic control." Plant Physiol 122(4);1193-9. PMID: 10759515

Qian94: Qian N, Stanley GA, Hahn-Hagerdal B, Radstrom P (1994). "Purification and characterization of two phosphoglucomutases from Lactococcus lactis subsp. lactis and their regulation in maltose- and glucose-utilizing cells." J Bacteriol 176(17);5304-11. PMID: 8071206

Ray64: Ray WJ, Roscelli GA (1964). "A kinetic study of the phosphoglucomutase pathway." J Biol Chem 239;1228-36. PMID: 14165931

Ray64a: Ray WJ Jr., Roscelli GA (1964). "A kinetic study of the phosphoglucomutase pathway." J Biol Chem 239:1228-1236.

Ray77: Ray WJ, Mildvan AS, Grutzner JB (1977). "Phosphorus nuclear magnetic resonance studies of phosphoglucomutase and its metal ion complexes." Arch Biochem Biophys 184(2);453-63. PMID: 23074

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Please cite the following article in publications resulting from the use of MetaCyc: Caspi et al, Nucleic Acids Research 42:D459-D471 2014
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