1887

Abstract

The biosynthesis of glycogen or starch is one of the main strategies developed by living organisms for the intracellular storage of carbon and energy. In phototrophic organisms, such polyglucans accumulate due to carbon fixation during photosynthesis and are used to provide maintenance energy for cell integrity, function and viability in dark periods. Moreover, it is assumed that glycogen enables cyanobacteria to cope with transient starvation conditions, as observed in most micro-organisms. Here, glycogen accumulates when an appropriate carbon source is available in sufficient amounts but growth is inhibited by lack of other nutrients. In this study, the role of glycogen in energy and carbon metabolism of phototrophic cyanobacteria was first analysed via a comparative physiological and metabolic characterization of knockout mutants defective in glycogen synthesis. We first proved the role of glycogen as a respiratory substrate in periods of darkness, the role of glycogen as a reserve to survive starvation periods such as nitrogen depletion and the role of glycogen synthesis as an ameliorator of carbon excess conditions in the model organism sp. PCC 6803. We provide striking new insights into the complex carbon and nitrogen metabolism of non-diazotrophic cyanobacteria: a phenotype of sensitivity to photomixotrophic conditions and of reduced glucose uptake, a non-bleaching phenotype based on an impaired acclimation response to nitrogen depletion and furthermore a phenotype of energy spilling. This study shows that the analysis of deficiencies in glycogen metabolism is a valuable tool for the identification of metabolic regulatory principles and signals.

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2012-12-01
2019-10-16
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References

  1. Aguirre von Wobeser E. , Ibelings B. W. , Bok J. , Krasikov V. , Huisman J. , Matthijs H. C. P. . ( 2011; ). Concerted changes in gene expression and cell physiology of the cyanobacterium Synechocystis sp. strain PCC 6803 during transitions between nitrogen and light-limited growth. . Plant Physiol 155:, 1445–1457. [CrossRef] [PubMed]
    [Google Scholar]
  2. Ball S. G. , Morell M. K. . ( 2003; ). From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. . Annu Rev Plant Biol 54:, 207–233. [CrossRef] [PubMed]
    [Google Scholar]
  3. Ball S. , Colleoni C. , Cenci U. , Raj J. N. , 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:, 1775–1801. [CrossRef] [PubMed]
    [Google Scholar]
  4. Beck C. , Knoop H. , Axmann I. M. , Steuer R. . ( 2012; ). The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms. . BMC Genomics 13:, 56. [CrossRef] [PubMed]
    [Google Scholar]
  5. Carr N. . ( 1988; ). Nitrogen reserves and dynamic reservoirs in cyanobacteria. . In Biochemistry of the Algae and Cyanobacteria, pp. 13–21. Edited by Rogers J. G. L. J. . . New York:: Oxford University Press;.
    [Google Scholar]
  6. Carrieri D. , Paddock T. , Maness P.-C. , Seibert M. , Yu J. . ( 2012; ). Photo-catalytic conversion of carbon dioxide to organic acids by a recombinant cyanobacterium incapable of glycogen storage. . Energy Environ Sci 5:, 9457–9461. [CrossRef]
    [Google Scholar]
  7. Cid E. , Geremia R. A. , Guinovart J. J. , Ferrer J. C. . ( 2002; ). Glycogen synthase: towards a minimum catalytic unit?. FEBS Lett 528:, 5–11. [CrossRef] [PubMed]
    [Google Scholar]
  8. Eichelmann H. , Laisk A. . ( 1994; ). CO2 uptake and electron-transport rates in wild-type and a starchless mutant of Nicotiana sylvestris (the role and regulation of starch synthesis at staturating CO2 concentrations). . Plant Physiol 106:, 679–687.[PubMed]
    [Google Scholar]
  9. Eisenhut M. , Huege J. , Schwarz D. , Bauwe H. , Kopka J. , Hagemann M. . ( 2008; ). Metabolome phenotyping of inorganic carbon limitation in cells of the wild type and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. . Plant Physiol 148:, 2109–2120. [CrossRef] [PubMed]
    [Google Scholar]
  10. Ermakova S. Y. , Elanskaya I. V. , Kallies K. U. , Weihe A. , Borner T. , Shestakov S. V. . ( 1993; ). Cloning and sequencing of mutant psbB genes of the cyanobacterium Synechocystis PCC 6803. . Photosynth Res 37:, 139–146. [CrossRef]
    [Google Scholar]
  11. Franche C. , Damerval T. . ( 1988; ). Tests on nif Probes and DNA Hybridizations. . In Cyanobacteria, pp. 803–808. Edited by Packer L. , Glazer A. N. . . San Diego, California:: Academic Press, Inc;. [CrossRef]
    [Google Scholar]
  12. Gill R. T. , Katsoulakis E. , Schmitt W. , Taroncher-Oldenburg G. , Misra J. , Stephanopoulos G. . ( 2002; ). Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. . J Bacteriol 184:, 3671–3681. [CrossRef] [PubMed]
    [Google Scholar]
  13. Grossman A. , McGowan R. E. . ( 1975; ). Regulation of glucose 6-phosphate dehydrogenase in blue-green algae. . Plant Physiol 55:, 658–662. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hagemann M. , Erdmann N. . ( 1994; ). Activation and pathway of glucosylglycerol synthesis in the cyanobacterium Synechocystis sp. PCC 6803. . Microbiology 140:, 1427–1431. [CrossRef]
    [Google Scholar]
  15. Huber S. C. , Hanson K. R. . ( 1992; ). Carbon partitiong and growth of a starchless mutant of Nicotiana sylvestris . . Plant Physiol 99:, 1449–1454. [CrossRef] [PubMed]
    [Google Scholar]
  16. Jansén T. , Kurian D. , Raksajit W. , York S. , Summers M. L. , Maenpaa P. . ( 2010; ). Characterization of trophic changes and a functional oxidative pentose phosphate pathway in Synechocystis sp. PCC 6803. . Acta Physiol Plant 32:, 511–518. [CrossRef]
    [Google Scholar]
  17. Kaplan A. , Hagemann M. , Bauwe H. , Kahlon S. , Ogawa T. . ( 2008; ). Carbon acquisition by cyanobacteria: mechanisms, comparative genomics, and evolution. . In The Cyanobacteria: Molecular Biology, Genomics and Evolution, pp. 305–334. Edited by Herrero A. , Flores E. . . Wymondham, UK:: Caister Academic Press;.
    [Google Scholar]
  18. Kaprelyants A. S. , Gottschal J. C. , Kell D. B. . ( 1993; ). Dormancy in non-sporulating bacteria. . FEMS Microbiol Rev 10:, 271–285.[PubMed] [CrossRef]
    [Google Scholar]
  19. Knoop H. , Zilliges Y. , Lockau W. , Steuer R. . ( 2010; ). The metabolic network of Synechocystis sp. PCC 6803: systemic properties of autotrophic growth. . Plant Physiol 154:, 410–422. [CrossRef] [PubMed]
    [Google Scholar]
  20. Koksharova O. , Schubert M. , Shestakov S. , Cerff R. . ( 1998; ). Genetic and biochemical evidence for distinct key functions of two highly divergent GAPDH genes in catabolic and anabolic carbon flow of the cyanobacterium Synechocystis sp. PCC 6803. . Plant Mol Biol 36:, 183–194. [CrossRef] [PubMed]
    [Google Scholar]
  21. Krasikov V. , Aguirre von Wobeser E. , Dekker H. L. , Huisman J. , Matthijs H. C. P. . ( 2012; ). Time-series resolution of gradual nitrogen starvation and its impact on photosynthesis in the cyanobacterium Synechocystis PCC 6803. . Physiol Plant 145:, 426–439. [CrossRef] [PubMed]
    [Google Scholar]
  22. Lahmi R. , Sendersky E. , Perelman A. , Hagemann M. , Forchhammer K. , Schwarz R. . ( 2006; ). Alanine dehydrogenase activity is required for adequate progression of phycobilisome degradation during nitrogen starvation in Synechococcus elongatus PCC 7942. . J Bacteriol 188:, 5258–5265. [CrossRef] [PubMed]
    [Google Scholar]
  23. Lamprecht W. , Heinz F. . ( 1984; ). Pyruvate. . In Methods of Enzymatic Analysis, pp. 570–577. Edited by Bergmeyer H. U. , Bergmeyer J. , Graßl M. . . Weinheim:: Verlag Chemie;.
    [Google Scholar]
  24. Lee S. , Ryu J.-Y. , Kim S. Y. , Jeon J. H. , Song J. Y. , Cho H. T. , Choi S. B. , Choi D. , de Marsac N. T. , Park Y. I. . ( 2007; ). Transcriptional regulation of the respiratory genes in the cyanobacterium Synechocystis sp. PCC 6803 during the early response to glucose feeding. . Plant Physiol 145:, 1018–1030. [CrossRef] [PubMed]
    [Google Scholar]
  25. Lindahl M. , Florencio F. J. . ( 2003; ). Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. . Proc Natl Acad Sci U S A 100:, 16107–16112. [CrossRef] [PubMed]
    [Google Scholar]
  26. Miao X. L. , Wu Q. Y. , Wu G. F. , Zhao N. M. . ( 2003a; ). Sucrose accumulation in salt-stressed cells of agp gene deletion-mutant in cyanobacterium Synechocystis sp PCC 6803. . FEMS Microbiol Lett 218:, 71–77. [CrossRef] [PubMed]
    [Google Scholar]
  27. Miao X. L. , Wu Q. Y. , Wu G. , Zhao N. . ( 2003b; ). Changes in photosynthesis and pigmentation in an agp deletion mutant of the cyanobacterium Synechocystis sp.. Biotechnol Lett 25:, 391–396. [CrossRef] [PubMed]
    [Google Scholar]
  28. Morrison S. S. , Mullineaux C. W. , Ashby M. K. . ( 2005; ). The influence of acetyl phosphate on DspA signalling in the cyanobacterium Synechocystis sp. PCC6803. . BMC Microbiol 5:, 47. [CrossRef] [PubMed]
    [Google Scholar]
  29. Nakao M. , Okamoto S. , Kohara M. , Fujishiro T. , Fujisawa T. , Sato S. , Tabata S. , Kaneko T. , Nakamura Y. . ( 2010; ). CyanoBase: the cyanobacteria genome database update 2010. . Nucleic Acids Res 38: (Database issue), D379–D381. [CrossRef] [PubMed]
    [Google Scholar]
  30. Nowack E. C. M. , Melkonian M. , Glöckner G. . ( 2008; ). Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. . Curr Biol 18:, 410–418. [CrossRef] [PubMed]
    [Google Scholar]
  31. Osanai T. , Azuma M. , Tanaka K. . ( 2007; ). Sugar catabolism regulated by light- and nitrogen-status in the cyanobacterium Synechocystis sp. PCC 6803. . Photochem Photobiol Sci 6:, 508–514. [CrossRef] [PubMed]
    [Google Scholar]
  32. Patron N. J. , Keeling P. J. . ( 2005; ). Common evolutionary origin of starch biosynthetic enzymes in green and red algae. . J Phycol 41:, 1131–1141. [CrossRef]
    [Google Scholar]
  33. Preiss J. . ( 1984; ). Bacterial glycogen synthesis and its regulation. . Annu Rev Microbiol 38:, 419–458. [CrossRef] [PubMed]
    [Google Scholar]
  34. Preiss J. , Romeo T. . ( 1994; ). Molecular biology and regulatory aspects of glycogen biosynthesis in bacteria. . Prog Nucleic Acid Res Mol Biol 47:, 299–329. [CrossRef] [PubMed]
    [Google Scholar]
  35. Rippka R. , Deruelles J. , Waterbury J. B. , Herdman M. , Stanier R. Y. . ( 1979; ). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. . J Gen Microbiol 111:, 1–61. [CrossRef]
    [Google Scholar]
  36. Russell J. B. . ( 2007; ). The energy spilling reactions of bacteria and other organisms. . J Mol Microbiol Biotechnol 13:, 1–11. [CrossRef] [PubMed]
    [Google Scholar]
  37. Russell J. B. , Cook G. M. . ( 1995; ). Energetics of bacterial growth: balance of anabolic and catabolic reactions. . Microbiol Rev 59:, 48–62.[PubMed]
    [Google Scholar]
  38. Ryu J. Y. , Song J. Y. , Lee J. M. , Jeong S. W. , Chow W. S. , Choi S. B. , Pogson B. J. , Park Y. I. . ( 2004; ). Glucose-induced expression of carotenoid biosynthesis genes in the dark is mediated by cytosolic pH in the cyanobacterium Synechocystis sp. PCC 6803. . J Biol Chem 279:, 25320–25325. [CrossRef] [PubMed]
    [Google Scholar]
  39. Sambrook J. , Fritsch E. , Maniatis T. . ( 1989; ). Molecular Cloning – a Laboratory Manual. New York:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  40. Schwarz R. , Forchhammer K. . ( 2005; ). Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. . Microbiology 151:, 2503–2514. [CrossRef] [PubMed]
    [Google Scholar]
  41. Senior P. J. . ( 1975; ). Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous-culture technique. . J Bacteriol 123:, 407–418.[PubMed]
    [Google Scholar]
  42. Smith A. J. . ( 1982; ). Modes of cyanobacterial carbon metabolism. . In The Biology of Cyanobacteria, pp. 47–85. Edited by Carr N. G. , Whitton B. A. . . Oxford:: Blackwell Scientific;.
    [Google Scholar]
  43. Stanier R. Y. , Cohen-Bazire G. . ( 1977; ). Phototrophic prokaryotes: the cyanobacteria. . Annu Rev Microbiol 31:, 225–274. [CrossRef] [PubMed]
    [Google Scholar]
  44. Sun J. D. , Okita T. W. , Edwards G. E. . ( 1999; ). Modification of carbon partitioning, photosynthetic capacity, and O2 sensitivity in Arabidopsis plants with low ADP-glucose pyrophosphorylase activity. . Plant Physiol 119:, 267–276. [CrossRef] [PubMed]
    [Google Scholar]
  45. Suzuki E. , Ohkawa H. , Moriya K. , Matsubara T. , Nagaike Y. , Iwasaki I. , Fujiwara S. , Tsuzuki M. , Nakamura Y. . ( 2010; ). Carbohydrate metabolism in mutants of the cyanobacterium Synechococcus elongatus PCC 7942 defective in glycogen synthesis. . Appl Environ Microbiol 76:, 3153–3159. [CrossRef] [PubMed]
    [Google Scholar]
  46. Tandeau de Marsac N. , Houmard J. . ( 1988; ). Complementary chromatic adaptation: physiological conditions and action spectra. . Methods in Enzymology, 167:, 318–328. [CrossRef]
    [Google Scholar]
  47. Taroncher-Oldenburg G. , Stephanopoulos G. . ( 2000; ). Targeted, PCR-based gene disruption in cyanobacteria: inactivation of the polyhydroxyalkanoic acid synthase genes in Synechocystis sp. PCC6803. . Appl Microbiol Biotechnol 54:, 677–680. [CrossRef] [PubMed]
    [Google Scholar]
  48. Teusink B. , Walsh M. C. , van Dam K. , Westerhoff H. V. . ( 1998; ). The danger of metabolic pathways with turbo design. . Trends Biochem Sci 23:, 162–169. [CrossRef] [PubMed]
    [Google Scholar]
  49. Wang L. , Wise M. J. . ( 2011; ). Glycogen with short average chain length enhances bacterial durability. . Naturwissenschaften 98:, 719–729. [CrossRef] [PubMed]
    [Google Scholar]
  50. Wilson W. A. , Roach P. J. , Montero M. , Baroja-Fernández E. , Muñoz F. J. , Eydallin G. , Viale A. M. , Pozueta-Romero J. . ( 2010; ). Regulation of glycogen metabolism in yeast and bacteria. . FEMS Microbiol Rev 34:, 952–985.[PubMed]
    [Google Scholar]
  51. Yoo S. H. , Spalding M. H. , Jane J. L. . ( 2002; ). Characterization of cyanobacterial glycogen isolated from the wild type and from a mutant lacking of branching enzyme. . Carbohydr Res 337:, 2195–2203. [CrossRef] [PubMed]
    [Google Scholar]
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