Skip to main content
PMC home page
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1997 Nov;63(11):4355–4359. doi: 10.1128/aem.63.11.4355-4359.1997

Glycogen biosynthesis via UDP-glucose in the ruminal bacterium Prevotella bryantii B1(4).

J Lou 1, K A Dawson 1, H J Strobel 1
PMCID: PMC168755  PMID: 9361422

Abstract

Prevotella bryantii is an important amylolytic bacterium in the rumen that produces considerable amounts of glycogen when it is grown on maltose. Radiolabel studies indicated that glucose-1-phosphate was converted to UDP-glucose, and this latter intermediate served as the immediate precursor for glycogen synthesis. High levels of UDP-glucose pyrophosphorylase activities (> 1,492 nmol/min/mg of protein) were detected in cells grown on maltose, cellobiose, glucose, or sucrose, and activity was greatly stimulated (by approximately 60-fold) by the addition of fructose-1,6-bis phosphate (half-maximal activation concentration was 240 microM). However, ADP-glucose pyrophosphorylase activity was not detected in any of the cultures. Glycogen synthase activity in maltose-grown cultures (48 nmol/min/mg of protein) was higher than that in cellobiose-, sucrose-, and glucose-grown cultures (< 26 nmol/min/mg of protein). This is the first report of a bacterium that exclusively uses UDP-glucose to synthesize glycogen. The elucidation of this unique glycogen biosynthesis pathway provides information necessary to further investigate the role of bacterial glycogen accumulation in rumen metabolism.

Full Text

The Full Text of this article is available as a PDF (238.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alonso M. D., Lomako J., Lomako W. M., Whelan W. J. A new look at the biogenesis of glycogen. FASEB J. 1995 Sep;9(12):1126–1137. doi: 10.1096/fasebj.9.12.7672505. [DOI] [PubMed] [Google Scholar]
  2. Avgustin G., Wallace R. J., Flint H. J. Phenotypic diversity among ruminal isolates of Prevotella ruminicola: proposal of Prevotella brevis sp. nov., Prevotella bryantii sp. nov., and Prevotella albensis sp. nov. and redefinition of Prevotella ruminicola. Int J Syst Bacteriol. 1997 Apr;47(2):284–288. doi: 10.1099/00207713-47-2-284. [DOI] [PubMed] [Google Scholar]
  3. BAILEY R. W. The reaction of pentoses with anthrone. Biochem J. 1958 Apr;68(4):669–672. doi: 10.1042/bj0680669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BRYANT M. P., SMALL N., BOUMA C., CHU H. Bacteroides ruminicola n. sp. and Succinimonas amylolytica; the new genus and species; species of succinic acid-producing anaerobic bacteria of the bovine rumen. J Bacteriol. 1958 Jul;76(1):15–23. doi: 10.1128/jb.76.1.15-23.1958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Costerton J. W., Damgaard H. N., Cheng K. J. Cell envelope morphology of rumen bacteria. J Bacteriol. 1974 Jun;118(3):1132–1143. doi: 10.1128/jb.118.3.1132-1143.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cotta M. A. Amylolytic activity of selected species of ruminal bacteria. Appl Environ Microbiol. 1988 Mar;54(3):772–776. doi: 10.1128/aem.54.3.772-776.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dietzler D. N., Leckie M. P., Lais C. J., Magnani J. L. Evidence for the allosteric regulation of glycogen synthesis in the intact Escherichia coli cell. Agreement of the values of the parameters of the Hill equation fitted to data for glycogen synthesis in vivo with the abailable values obtained in vitro with adenosine diphosphoglucose synthetase. J Biol Chem. 1975 Mar 25;250(6):2383–2387. [PubMed] [Google Scholar]
  8. Fontana J. D., Krisman C. R. Glycogen synthesis in the fungus Neurospora crassa. Biochim Biophys Acta. 1978 May 3;540(2):183–189. doi: 10.1016/0304-4165(78)90130-7. [DOI] [PubMed] [Google Scholar]
  9. GOLDEMBERG S. H. Specificity of uridine diphosphate glucose-glycogen glucosyltransferase. Biochim Biophys Acta. 1962 Jan 29;56:357–359. doi: 10.1016/0006-3002(62)90576-0. [DOI] [PubMed] [Google Scholar]
  10. GREENBERG E., PREISS J. THE OCCURRENCE OF ADENOSINE DIPHOSPHATE GLUCOSE: GLYCOGEN TRANSGLUCOSYLASE IN BACTERIA. J Biol Chem. 1964 Dec;239:4314–4315. [PubMed] [Google Scholar]
  11. Gaudet G., Forano E., Dauphin G., Delort A. M. Futile cycling of glycogen in Fibrobacter succinogenes as shown by in situ 1H-NMR and 13C-NMR investigation. Eur J Biochem. 1992 Jul 1;207(1):155–162. doi: 10.1111/j.1432-1033.1992.tb17032.x. [DOI] [PubMed] [Google Scholar]
  12. Govons S., Gentner N., Greenberg E., Preiss J. Biosynthesis of bacterial glycogen. XI. Kinetic characterization of an altered adenosine diphosphate-glucose synthase from a "glycogen-excess" mutant of Escherichia coli B. J Biol Chem. 1973 Mar 10;248(5):1731–1740. [PubMed] [Google Scholar]
  13. Howlett M. R., Mountfort D. O., Turner K. W., Roberton A. M. Metabolism and growth yields in Bacteroides ruminicola strain b14. Appl Environ Microbiol. 1976 Aug;32(2):274–283. doi: 10.1128/aem.32.2.274-283.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kiel J. A., Boels J. M., Beldman G., Venema G. Glycogen in Bacillus subtilis: molecular characterization of an operon encoding enzymes involved in glycogen biosynthesis and degradation. Mol Microbiol. 1994 Jan;11(1):203–218. doi: 10.1111/j.1365-2958.1994.tb00301.x. [DOI] [PubMed] [Google Scholar]
  15. Konishi Y., Tanizawa K., Muroya S., Fukui T. Molecular cloning, nucleotide sequencing, and affinity labeling of bovine liver UDP-glucose pyrophosphorylase. J Biochem. 1993 Jul;114(1):61–68. doi: 10.1093/oxfordjournals.jbchem.a124141. [DOI] [PubMed] [Google Scholar]
  16. LELOIR L. F., OLAVARRIA J. M., GOLDEMBERG S. H., CARMINATTI H. Biosynthesis of glycogen from uridine diphosphate glucose. Arch Biochem Biophys. 1959 Apr;81(2):508–520. doi: 10.1016/0003-9861(59)90232-2. [DOI] [PubMed] [Google Scholar]
  17. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  18. Lou J., Dawson K. A., Strobel H. J. Glycogen Formation by the Ruminal Bacterium Prevotella ruminicola. Appl Environ Microbiol. 1997 Apr;63(4):1483–1488. doi: 10.1128/aem.63.4.1483-1488.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lou J., Dawson K. A., Strobel H. J. Role of phosphorolytic cleavage in cellobiose and cellodextrin metabolism by the ruminal bacterium Prevotella ruminicola. Appl Environ Microbiol. 1996 May;62(5):1770–1773. doi: 10.1128/aem.62.5.1770-1773.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Peng H. L., Chang H. Y. Cloning of a human liver UDP-glucose pyrophosphorylase cDNA by complementation of the bacterial galU mutation. FEBS Lett. 1993 Aug 23;329(1-2):153–158. doi: 10.1016/0014-5793(93)80213-e. [DOI] [PubMed] [Google Scholar]
  21. Preiss J. Bacterial glycogen synthesis and its regulation. Annu Rev Microbiol. 1984;38:419–458. doi: 10.1146/annurev.mi.38.100184.002223. [DOI] [PubMed] [Google Scholar]
  22. Preiss J., Romeo T. Molecular biology and regulatory aspects of glycogen biosynthesis in bacteria. Prog Nucleic Acid Res Mol Biol. 1994;47:299–329. doi: 10.1016/s0079-6603(08)60255-x. [DOI] [PubMed] [Google Scholar]
  23. Preiss J., Romeo T. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv Microb Physiol. 1989;30:183–238. doi: 10.1016/s0065-2911(08)60113-7. [DOI] [PubMed] [Google Scholar]
  24. Roach P. J. Control of glycogen synthase by hierarchal protein phosphorylation. FASEB J. 1990 Sep;4(12):2961–2968. [PubMed] [Google Scholar]
  25. Russell J. B., Dombrowski D. B. Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Appl Environ Microbiol. 1980 Mar;39(3):604–610. doi: 10.1128/aem.39.3.604-610.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Russell J. B. Fermentation of cellodextrins by cellulolytic and noncellulolytic rumen bacteria. Appl Environ Microbiol. 1985 Mar;49(3):572–576. doi: 10.1128/aem.49.3.572-576.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Russell J. B. Glucose toxicity and inability of Bacteroides ruminicola to regulate glucose transport and utilization. Appl Environ Microbiol. 1992 Jun;58(6):2040–2045. doi: 10.1128/aem.58.6.2040-2045.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Russell J. B. Glucose toxicity in Prevotella ruminicola: methylglyoxal accumulation and its effect on membrane physiology. Appl Environ Microbiol. 1993 Sep;59(9):2844–2850. doi: 10.1128/aem.59.9.2844-2850.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shah H. N., Collins D. M. Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. Int J Syst Bacteriol. 1990 Apr;40(2):205–208. doi: 10.1099/00207713-40-2-205. [DOI] [PubMed] [Google Scholar]
  30. Skurat A. V., Peng H. L., Chang H. Y., Cannon J. F., Roach P. J. Rate-determining steps in the biosynthesis of glycogen in COS cells. Arch Biochem Biophys. 1996 Apr 15;328(2):283–288. doi: 10.1006/abbi.1996.0174. [DOI] [PubMed] [Google Scholar]
  31. Sowokinos J. R. Pyrophosphorylases in Solanum tuberosum: I. Changes in ADP-Glucose and UDP-Glucose Pyrophosphorylase Activities Associated with Starch Biosynthesis during Tuberization, Maturation, and Storage of Potatoes. Plant Physiol. 1976 Jan;57(1):63–68. doi: 10.1104/pp.57.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Strobel H. J. Evidence for catabolite inhibition in regulation of pentose utilization and transport in the ruminal bacterium Selenomonas ruminantium. Appl Environ Microbiol. 1993 Jan;59(1):40–46. doi: 10.1128/aem.59.1.40-46.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Varón D., Boylan S. A., Okamoto K., Price C. W. Bacillus subtilis gtaB encodes UDP-glucose pyrophosphorylase and is controlled by stationary-phase transcription factor sigma B. J Bacteriol. 1993 Jul;175(13):3964–3971. doi: 10.1128/jb.175.13.3964-3971.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES