1887

Abstract

Using metabolic and transcriptomic phenotyping, we studied acclimation of cyanobacteria to low inorganic carbon (LC) conditions and the requirements for coordinated alteration of metabolism and gene expression. To analyse possible metabolic signals for LC sensing and compensating reactions, the carboxysome-less mutant Δ and the photorespiratory mutant Δ/ were compared with wild-type (WT) . Metabolic phenotyping revealed accumulation of 2-phosphoglycolate (2PG) in Δ and of glycolate in Δ/ in LC- but also in high inorganic carbon (HC)-grown mutant cells. The accumulation of photorespiratory metabolites provided evidence for the oxygenase activity of RubisCO at HC. The global gene expression patterns of HC-grown Δ and Δ/ showed differential expression of many genes involved in photosynthesis, high-light stress and N assimilation. In contrast, the transcripts of LC-specific genes, such as those for inorganic carbon transporters and components of the carbon-concentrating mechanism (CCM), remained unchanged in HC cells. After a shift to LC, Δ/ and WT cells displayed induction of many of the LC-inducible genes, whereas Δ lacked similar changes in expression. From the coincidence of the presence of 2PG in Δ without CCM induction and of glycolate in Δ/ with CCM induction, we regard a direct role for 2PG as a metabolic signal for the induction of CCM during LC acclimation as less likely. Instead, our data suggest a potential role for glycolate as a signal molecule for enhanced expression of CCM genes.

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2012-02-01
2019-10-23
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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. Badger M. R. . ( 1980; ). Kinetic properties of ribulose 1,5-bisphosphate carboxylase/oxygenase from Anabaena variabilis . . Arch Biochem Biophys 201:, 247–254. [CrossRef] [PubMed]
    [Google Scholar]
  3. Badger M. R. , Price G. D. , Long B. M. , Woodger F. J. . ( 2006; ). The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. . J Exp Bot 57:, 249–265. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bauwe H. , Hagemann M. , Fernie A. R. . ( 2010; ). Photorespiration: players, partners and origin. . Trends Plant Sci 15:, 330–336. [CrossRef] [PubMed]
    [Google Scholar]
  5. Berry S. , Fischer J. H. , Kruip J. , Hauser M. , Wildner G. F. . ( 2005; ). Monitoring cytosolic pH of carboxysome-deficient cells of Synechocystis sp. PCC 6803 using fluorescence analysis. . Plant Biol (Stuttg) 7:, 342–347. [CrossRef] [PubMed]
    [Google Scholar]
  6. Dietz K.-J. , Pfannschmidt T. . ( 2011; ). Novel regulators in photosynthetic redox control of plant metabolism and gene expression. . Plant Physiol 155:, 1477–1485. [CrossRef] [PubMed]
    [Google Scholar]
  7. Eisenhut M. , von Wobeser E. A. , Jonas L. , Schubert H. , Ibelings B. W. , Bauwe H. , Matthijs H. C. P. , Hagemann M. . ( 2007; ). Long-term response toward inorganic carbon limitation in wild type and glycolate turnover mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. . Plant Physiol 144:, 1946–1959. [CrossRef] [PubMed]
    [Google Scholar]
  8. Eisenhut M. , Ruth W. , Haimovich M. , Bauwe H. , Kaplan A. , Hagemann M. . ( 2008a; ). The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. . Proc Natl Acad Sci U S A 105:, 17199–17204. [CrossRef] [PubMed]
    [Google Scholar]
  9. Eisenhut M. , Huege J. , Schwarz D. , Bauwe H. , Kopka J. , Hagemann M. . ( 2008b; ). 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. Figge R. M. , Cassier-Chauvat C. , Chauvat F. , Cerff R. . ( 2001; ). Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. . Mol Microbiol 39:, 455–468. [CrossRef] [PubMed]
    [Google Scholar]
  11. García-Domínguez M. , Lopez-Maury L. , Florencio F. J. , Reyes J. C. . ( 2000; ). A gene cluster involved in metal homeostasis in the cyanobacterium Synechocystis sp. strain PCC 6803. . J Bacteriol 182:, 1507–1514. [CrossRef] [PubMed]
    [Google Scholar]
  12. Hackenberg C. , Engelhardt A. , Matthijs H. C. P. , Wittink F. , Bauwe H. , Kaplan A. , Hagemann M. . ( 2009; ). Photorespiratory 2-phosphoglycolate metabolism and photoreduction of O2 cooperate in high-light acclimation of Synechocystis sp. strain PCC 6803. . Planta 230:, 625–637. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hagemann M. , Schoor A. , Jeanjean R. , Zuther E. , Joset F. . ( 1997; ). The stpA gene from Synechocystis sp. strain PCC 6803 encodes the glucosylglycerol-phosphate phosphatase involved in cyanobacterial osmotic response to salt shock. . J Bacteriol 179:, 1727–1733.[PubMed]
    [Google Scholar]
  14. Hetherington A. M. , Raven J. A. . ( 2005; ). The biology of carbon dioxide. . Curr Biol 15:, R406–R410. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hihara Y. , Kamei A. , Kanehisa M. , Kaplan A. , Ikeuchi M. . ( 2001; ). DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. . Plant Cell 13:, 793–806. [CrossRef] [PubMed]
    [Google Scholar]
  16. Huege J. , Goetze J. , Schwarz D. , Bauwe H. , Hagemann M. , Kopka J. . ( 2011; ). Modulation of the major paths of carbon in photorespiratory mutants of Synechocystis . . PLoS ONE 6:, e16278. [CrossRef] [PubMed]
    [Google Scholar]
  17. Imlay J. A. . ( 2006; ). Iron–sulphur clusters and the problem with oxygen. . Mol Microbiol 59:, 1073–1082. [CrossRef] [PubMed]
    [Google Scholar]
  18. 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. . . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  19. Kelly G. J. , Latzko E. . ( 1977; ). Chloroplast phosphofructokinase: II. Partial purification, kinetic and regulatory properties. . Plant Physiol 60:, 295–299. [CrossRef] [PubMed]
    [Google Scholar]
  20. 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]
  21. Li H. , Singh A. K. , McIntyre L. M. , Sherman L. A. . ( 2004; ). Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. . J Bacteriol 186:, 3331–3345. [CrossRef] [PubMed]
    [Google Scholar]
  22. Lieman-Hurwitz J. , Haimovich M. , Shalev-Malul G. , Ishii A. , Hihara Y. , Gaathon A. , Lebendiker M. , Kaplan A. . ( 2009; ). A cyanobacterial AbrB-like protein affects the apparent photosynthetic affinity for CO2 by modulating low-CO2-induced gene expression. . Environ Microbiol 11:, 927–936. [CrossRef] [PubMed]
    [Google Scholar]
  23. Los D. , Suzuki I. , Zinchenko V. , Murata N. . ( 2008; ). Stress responses in Synechocystis: regulated genes and regulatory systems. . In The Cyanobacteria: Molecular Biology, Genomics and Evolution, pp. 115–157. Edited by Herrero A. , Flores E. . . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  24. Marcus Y. , Harel E. , Kaplan A. . ( 1983; ). Adaptation of the cyanobacterium Anabaena variabilis to low CO2 concentration in their environment. . Plant Physiol 71:, 208–210. [CrossRef] [PubMed]
    [Google Scholar]
  25. McGinn P. , Price G. , Badger M. . ( 2004; ). High light enhances the expression of low-CO2-inducible transcripts involved in the CO2-concentrating mechanism in Synechocystis sp. PCC6803. . Plant Cell Environ 27:, 615–626. [CrossRef]
    [Google Scholar]
  26. Nishimura T. , Takahashi Y. , Yamaguchi O. , Suzuki H. , Maeda S. , Omata T. . ( 2008; ). Mechanism of low CO2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. . Mol Microbiol 68:, 98–109. [CrossRef] [PubMed]
    [Google Scholar]
  27. Norman E. G. , Colman B. . ( 1991; ). Purification and characterization of phosphoglycolate phosphatase from the cyanobacterium Coccochloris peniocystis . . Plant Physiol 95:, 693–698. [CrossRef] [PubMed]
    [Google Scholar]
  28. Ogawa T. , Amichay D. , Gurevitz M. . ( 1994; ). Isolation and characterization of the ccmM gene required by the cyanobacterium Synechocystis PCC6803 for inorganic carbon utilization. . Photosynth Res 39:, 183–190. [CrossRef]
    [Google Scholar]
  29. Osanai T. , Imamura S. , Asayama M. , Shirai M. , Suzuki I. , Murata N. , Tanaka K. . ( 2006; ). Nitrogen induction of sugar catabolic gene expression in Synechocystis sp. PCC 6803. . DNA Res 13:, 185–195. [CrossRef] [PubMed]
    [Google Scholar]
  30. Rippka R. , Deruelles J. , Waterbury J. , Herdman M. , Stanier R. . ( 1979; ). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. . J Gen Microbiol 111:, 1–61.[CrossRef]
    [Google Scholar]
  31. Schwarz D. , Nodop A. , Hüge J. , Purfürst S. , Forchhammer K. , Michel K. P. , Bauwe H. , Kopka J. , Hagemann M. . ( 2011; ). Metabolic and transcriptomic phenotyping of inorganic carbon acclimation in the cyanobacterium Synechococcus elongatus PCC 7942. . Plant Physiol 155:, 1640–1655. [CrossRef] [PubMed]
    [Google Scholar]
  32. Suzuki I. , Kanesaki Y. , Hayashi H. , Hall J. J. , Simon W. J. , Slabas A. R. , Murata N. . ( 2005; ). The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis . . Plant Physiol 138:, 1409–1421. [CrossRef] [PubMed]
    [Google Scholar]
  33. Tamoi M. , Miyazaki T. , Fukamizo T. , Shigeoka S. . ( 2005; ). The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. . Plant J 42:, 504–513. [CrossRef] [PubMed]
    [Google Scholar]
  34. Tcherkez G. G. B. , Farquhar G. D. , Andrews T. J. . ( 2006; ). Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. . Proc Natl Acad Sci U S A 103:, 7246–7251. [CrossRef] [PubMed]
    [Google Scholar]
  35. Tchernov D. , Silverman J. , Luz B. , Reinhold L. , Kaplan A. . ( 2003; ). Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings. . Photosynth Res 77:, 95–103. [CrossRef] [PubMed]
    [Google Scholar]
  36. Wang H. L. , Postier B. L. , Burnap R. L. . ( 2004; ). Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. . J Biol Chem 279:, 5739–5751. [CrossRef] [PubMed]
    [Google Scholar]
  37. Wedel N. , Soll J. . ( 1998; ). Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/glyceraldehyde-3-phosphate dehydrogenase complex dissociation. . Proc Natl Acad Sci U S A 95:, 9699–9704. [CrossRef] [PubMed]
    [Google Scholar]
  38. Woodger F. J. , Badger M. R. , Price G. D. . ( 2005; ). Sensing of inorganic carbon limitation in Synechococcus PCC7942 is correlated with the size of the internal inorganic carbon pool and involves oxygen. . Plant Physiol 139:, 1959–1969. [CrossRef] [PubMed]
    [Google Scholar]
  39. Yeates T. O. , Kerfeld C. A. , Heinhorst S. , Cannon G. C. , Shively J. M. . ( 2008; ). Protein-based organelles in bacteria: carboxysomes and related microcompartments. . Nat Rev Microbiol 6:, 681–691. [CrossRef] [PubMed]
    [Google Scholar]
  40. Zhang P. , Allahverdiyeva Y. , Eisenhut M. , Aro E. M. . ( 2009; ). Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. . PLoS ONE 4:, e5331. [CrossRef] [PubMed]
    [Google Scholar]
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