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Abstract

Glycogen, a large α-glucan, is a ubiquitous energy storage molecule among bacteria, and its biosynthesis by the classical GlgC-GlgA pathway and its degradation have long been well understood – or so we thought. A second pathway of α-glucan synthesis, the four-step GlgE pathway, was recently discovered in mycobacteria. It requires trehalose as a precursor, and has been genetically validated as a novel anti-tuberculosis drug target. The ability to convert glycogen into trehalose was already known, so the GlgE pathway provides a complementary way of cycling these two metabolites. As well as containing cytosolic storage glycogen, mycobacteria possess an outer capsule containing a glycogen-like α-glucan that is implicated in immune system evasion, so the GlgE pathway might be linked to capsular α-glucan biosynthesis. Another pathway (the Rv3032 pathway) for α-glucan biosynthesis in mycobacteria generates a methylglucose lipopolysaccharide thought to be associated with fatty acid metabolism. A comparative genomic analysis was carried out to evaluate the occurrence and role of the classical pathway, the new GlgE pathway and the Rv3032 pathway across bacteria occupying very different ecological niches. The GlgE pathway is represented in 14 % of sequenced genomes from diverse bacteria (about half as common as the classical pathway), while the Rv3032 pathway is restricted with few exceptions to mycobacteria, and the GlgB branching enzyme, usually presumed to be associated with the classical pathway, correlates more strongly with the new GlgE pathway. The microbiological implications of recent discoveries in the light of the comparative genomic analysis are discussed.

Funding
This study was supported by the:
  • United Kingdon Biotechnology and Biological Sciences Research Council (Award MET Institute Strategic Programme Grant)
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2011-06-01
2024-04-20
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References

  1. Argüelles J. C. ( 2000). Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174:217–224 [View Article][PubMed]
    [Google Scholar]
  2. Belanger A. E., Hatfull G. F. ( 1999). Exponential-phase glycogen recycling is essential for growth of Mycobacterium smegmatis . J Bacteriol 181:6670–6678[PubMed]
    [Google Scholar]
  3. Cantarel B. L., Coutinho P. M., Rancurel C., Bernard T., Lombard V., Henrissat B. ( 2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:Database issueD233–D238 [View Article][PubMed]
    [Google Scholar]
  4. Carroll J. D., Pastuszak I., Edavana V. K., Pan Y. T., Elbein A. D. ( 2007). A novel trehalase from Mycobacterium smegmatis – purification, properties, requirements. FEBS J 274:1701–1714 [View Article][PubMed]
    [Google Scholar]
  5. Dinadayala P., Sambou T., Daffé M., Lemassu A. ( 2008). Comparative structural analyses of the α-glucan and glycogen from Mycobacterium bovis . Glycobiology 18:502–508 [View Article][PubMed]
    [Google Scholar]
  6. Elbein A. D., Pan Y. T., Pastuszak I., Carroll D. ( 2003). New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R [View Article][PubMed]
    [Google Scholar]
  7. Elbein A. D., Pastuszak I., Tackett A. J., Wilson T., Pan Y. T. ( 2010). Last step in the conversion of trehalose to glycogen: a mycobacterial enzyme that transfers maltose from maltose 1-phosphate to glycogen. J Biol Chem 285:9803–9812 [View Article][PubMed]
    [Google Scholar]
  8. Freeman B. C., Chen C. L., Beattie G. A. ( 2010). Identification of the trehalose biosynthetic loci of Pseudomonas syringae and their contribution to fitness in the phyllosphere. Environ Microbiol 12:1486–1497[PubMed]
    [Google Scholar]
  9. Gagliardi M. C., Lemassu A., Teloni R., Mariotti S., Sargentini V., Pardini M., Daffé M., Nisini R. ( 2007). Cell wall-associated α-glucan is instrumental for Mycobacterium tuberculosis to block CD1 molecule expression and disable the function of dendritic cell derived from infected monocyte. Cell Microbiol 9:2081–2092 [View Article][PubMed]
    [Google Scholar]
  10. Jackson M., Brennan P. J. ( 2009). Polymethylated polysaccharides from Mycobacterium species revisited. J Biol Chem 284:1949–1953 [View Article][PubMed]
    [Google Scholar]
  11. Jarling M., Cauvet T., Grundmeier M., Kuhnert K., Pape H. ( 2004). Isolation of mak1 from Actinoplanes missouriensis and evidence that Pep2 from Streptomyces coelicolor is a maltokinase. J Basic Microbiol 44:360–373 [View Article][PubMed]
    [Google Scholar]
  12. Kalscheuer R., Syson K., Veeraraghavan U., Weinrick B., Biermann K. E., Liu Z., Sacchettini J. C., Besra G., Bornemann S., Jacobs W. R. Jr ( 2010). Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an α-glucan pathway. Nat Chem Biol 6:376–384 [View Article][PubMed]
    [Google Scholar]
  13. Kaur D., Guerin M. E., Škovierová H., Brennan P. J., Jackson M. ( 2009a). Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis . Advances in Applied Microbiology23–77 Laskin A., Gadd G., Sariaslani S. Amsterdam: Elsevier;
    [Google Scholar]
  14. Kaur D., Pham H., Larrouy-Maumus G., Rivière M., Vissa V., Guerin M. E., Puzo G., Brennan P. J., Jackson M. ( 2009b). Initiation of methylglucose lipopolysaccharide biosynthesis in mycobacteria. PLoS ONE 4:e5447 [View Article][PubMed]
    [Google Scholar]
  15. Lee Y. C. ( 1966). Isolation and characterization of lipopolysaccharides containing 6-O-methyl-d-glucose from Mycobacterium species. J Biol Chem 241:1899–1908[PubMed]
    [Google Scholar]
  16. Martin M. C., Schneider D., Bruton C. J., Chater K. F., 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]
    [Google Scholar]
  17. Maruta K., Mitsuzumi H., Nakada T., Kubota M., Chaen H., Fukuda S., Sugimoto T., Kurimoto M. ( 1996). Cloning and sequencing of a cluster of genes encoding novel enzymes of trehalose biosynthesis from thermophilic archaebacterium Sulfolobus acidocaldarius . Biochim Biophys Acta 1291:177–181[PubMed] [CrossRef]
    [Google Scholar]
  18. McBride M. J., Ensign J. C. ( 1987). Metabolism of endogenous trehalose by Streptomyces griseus spores and by spores or cells of other actinomycetes. J Bacteriol 169:5002–5007[PubMed]
    [Google Scholar]
  19. McBride M. J., Ensign J. C. ( 1990). Regulation of trehalose metabolism by Streptomyces griseus spores. J Bacteriol 172:3637–3643[PubMed]
    [Google Scholar]
  20. Murakami T., Kanai T., Takata H., Kuriki T., Imanaka T. ( 2006). A novel branching enzyme of the GH-57 family in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol 188:5915–5924 [View Article][PubMed]
    [Google Scholar]
  21. Nandi T., Ong C., Singh A. P., Boddey J., Atkins T., Sarkar-Tyson M., Essex-Lopresti A. E., Chua H. H., Pearson T. et al. ( 2010). A genomic survey of positive selection in Burkholderia pseudomallei provides insights into the evolution of accidental virulence. PLoS Pathog 6:e1000845 [View Article][PubMed]
    [Google Scholar]
  22. Nishimoto T., Nakano M., Nakada T., Chaen H., Fukuda S., Sugimoto T., Kurimoto M., Tsujisaka Y. ( 1996). Purification and properties of a novel enzyme, trehalose synthase, from Pimelobacter sp. R48. Biosci Biotechnol Biochem 60:640–644 [View Article][PubMed]
    [Google Scholar]
  23. Palomo M., Pijning T., Booiman T., Dobruchowska J. M., van der Vlist J., Kralj S., Planas A., Loos K., Kamerling J. P. et al. ( 2011). Thermus thermophilus glycoside hydrolase family 57 branching enzyme: crystal structure, mechanism of action, and products formed. J Biol Chem 286:3520–3530 [View Article][PubMed]
    [Google Scholar]
  24. Pan Y. T., Koroth Edavana V., Jourdian W. J., Edmondson R., Carroll J. D., Pastuszak I., Elbein A. D. ( 2004). Trehalose synthase of Mycobacterium smegmatis: purification, cloning, expression, and properties of the enzyme. Eur J Biochem 271:4259–4269 [View Article][PubMed]
    [Google Scholar]
  25. Plaskitt K. A., Chater K. F. ( 1995). Influences of developmental genes on localized glycogen deposition in colonies of a mycelial prokaryote, Streptomyces coelicolor A3(2) – a possible interface between metabolism and mophogenesis. Philos Trans R Soc Lond B Biol Sci 347:105–121 [View Article]
    [Google Scholar]
  26. Pommier M. T., Michel G. ( 1986). Isolation and characterization of an O-methylglucose-containing lipopolysaccharide produced by Nocardia otitidis-caviarum . J Gen Microbiol 132:2433–2441[PubMed]
    [Google Scholar]
  27. Preiss J. ( 2006). Bacterial glycogen inclusions: enzymology and regulation of synthesis. Microbiology Monographs71–108 Shively J. M. Heidelberg, Germany: Springer;
    [Google Scholar]
  28. Preiss J. ( 2009). Glycogen biosynthesis. The Encyclopedia of Microbiology vol. 5145–158 Schaechter M. Oxford, UK: Elsevier; [View Article]
    [Google Scholar]
  29. Preiss J., Romeo T. ( 1989). Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv Microb Physiol 30:183–238 [View Article][PubMed]
    [Google Scholar]
  30. Reysenbach A. L., Ravenscroft N., Long S., Jones D. T., Woods D. R. ( 1986). Characterization, biosynthesis, and regulation of granulose in Clostridium acetobutylicum . Appl Environ Microbiol 52:185–190[PubMed]
    [Google Scholar]
  31. Rueda B., Miguélez E. M., Hardisson C., Manzanal M. B. ( 2001). Changes in glycogen and trehalose content of Streptomyces brasiliensis hyphae during growth in liquid cultures under sporulating and non-sporulating conditions. FEMS Microbiol Lett 194:181–185 [View Article][PubMed]
    [Google Scholar]
  32. Sambou T., Dinadayala P., Stadthagen G., Barilone N., Bordat Y., Constant P., Levillain F., Neyrolles O., Gicquel B. et al. ( 2008). Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and impact on the persistence in mice. Mol Microbiol 70:762–774 [View Article][PubMed]
    [Google Scholar]
  33. Schneider D., Bruton C. J., Chater K. F. ( 2000). Duplicated gene clusters suggest an interplay of glycogen and trehalose metabolism during sequential stages of aerial mycelium development in Streptomyces coelicolor A3(2). Mol Gen Genet 263:543–553 [View Article][PubMed]
    [Google Scholar]
  34. Stadthagen G., Sambou T., Guerin M., Barilone N., Boudou F., Korduláková J., Charles P., Alzari P. M., Lemassu A. et al. ( 2007). Genetic basis for the biosynthesis of methylglucose lipopolysaccharides in Mycobacterium tuberculosis . J Biol Chem 282:27270–27276 [View Article][PubMed]
    [Google Scholar]
  35. Takayama K., Wang C., Besra G. S. ( 2005). Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis . Clin Microbiol Rev 18:81–101 [View Article][PubMed]
    [Google Scholar]
  36. Yeo M., Chater K. ( 2005). The interplay of glycogen metabolism and differentiation provides an insight into the developmental biology of Streptomyces coelicolor . Microbiology 151:855–861 [View Article][PubMed]
    [Google Scholar]
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