1887

Abstract

Inactivation of the gene (), encoding the group 2 sigma factor SigC, leads to a heat-sensitive phenotype of sp. PCC 6803. Cells of the ΔsigC strain grew poorly at 43 °C at pH 7.5 under ambient CO conditions. Addition of inorganic carbon in the form of 3 % CO or use of an alkaline growth medium (pH 8.3) restored the growth of the ΔsigC strain at 43 °C. These treatments compensate for the low concentration of inorganic carbon at high temperature. However, addition of organic carbon as glucose, pyruvate, succinate or 2-oxoglutarate did not restore growth of the ΔsigC strain at 43 °C. In the control strain, the amount of the SigC factor diminished after prolonged incubation at 43 °C if the pH of the growth medium was 7.5 or 6.7. Under alkaline conditions, the amount of the SigC factor remained constant at 43 °C and cells of the control strain grew better than at pH 7.5 or pH 6.7. The pH dependence of high-temperature growth was associated with changes in photosynthetic activity, indicating that the SigC factor is involved in adjustment of photosynthesis according to the amount of available inorganic carbon. Our results indicate that acclimation to low inorganic carbon is a part of acclimation to prolonged high temperature and that the SigC factor has a central role in this acclimation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032565-0
2010-01-01
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/1/220.html?itemId=/content/journal/micro/10.1099/mic.0.032565-0&mimeType=html&fmt=ahah

References

  1. Asayama M., Imamura S. 2008; Stringent promoter recognition and autoregulation by the group 3 σ-factor SigF in the cyanobacterium Synechocystis sp. strain PCC 6803. Nucleic Acids Res 36:5297–5305
    [Google Scholar]
  2. Asayama M., Imamura S., Yoshihara S., Miyazaki A., Yoshida N., Sazuka T., Kaneko T., Ohara O., Tabata S. other authors 2004; SigC, the group 2 sigma factor of RNA polymerase, contributes to the late-stage gene expression and nitrogen promoter recognition in the cyanobacterium Synechocystis sp. strain PCC 6803. Biosci Biotechnol Biochem 68:477–487
    [Google Scholar]
  3. Bhaya D., Watanabe N., Ogawa T., Grossman A. R. 1999; The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC6803. Proc Natl Acad Sci U S A 96:3188–3193
    [Google Scholar]
  4. Bhaya D., Nakasugi K., Fazeli F., Burriesci M. S. 2006; Phototaxis and impaired motility in adenylyl cyclase and cyclase receptor protein mutants of Synechocystis sp. strain PCC 6803. J Bacteriol 188:7306–7310
    [Google Scholar]
  5. Eaton-Rye J. J., Shand J. A., Nicoll W. S. 2003; pH-dependent photoautotrophic growth of specific photosystem II mutants lacking lumenal extrinsic polypeptide in Synechocystis PCC 6803. FEBS Lett 543:148–153
    [Google Scholar]
  6. Foster J. S., Singh A. K., Rothschild L. J., Sherman L. A. 2007; Growth-phase dependent differential gene expression in Synechocystis sp. strain PCC 6803 and regulation by a group 2 sigma factor. Arch Microbiol 187:265–279
    [Google Scholar]
  7. Gruber T. M., Bryant D. A. 1998; Characterization of the alternative σ-factors SigD and SigE in Synechococcus sp. strain PCC 7002. SigE is implicated in transcription of post-exponential-phase-specific genes. Arch Microbiol 169:211–219
    [Google Scholar]
  8. Huang L., McCluskey M. P., Ni H., LaRossa R. A. 2002; Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J Bacteriol 184:6845–6858
    [Google Scholar]
  9. Imamura S., Yoshihara S., Nakano S., Shiozaki N., Yamada A., Tanaka K., Takahashi H., Asayama M., Shirai M. 2003; Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium. J Mol Biol 325:857–872
    [Google Scholar]
  10. Imamura S., Tanaka K., Shirai M., Asayama M. 2006; Growth phase-dependent activation of nitrogen-related genes by a control network of group 1 and group 2 σ factors in a cyanobacterium. J Biol Chem 281:2668–2675
    [Google Scholar]
  11. Inoue N., Taira Y., Emi T., Yamane Y., Kashino Y., Koike H., Satoh K. 2001; Acclimation to the growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant Cell Physiol 42:1140–1148
    [Google Scholar]
  12. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M. other authors 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136
    [Google Scholar]
  13. Laurent S., Jang J., Janicki A., Zhang C.-C., Bédu S. 2008; Inactivation of spkD, encoding a Ser/Thr kinase, affects the pool of the TCA cycle metabolites in Synechocystis sp. strain PCC 6803. Microbiology 154:2161–2167
    [Google Scholar]
  14. Lee S., Owen H. A., Prochaska D. J., Barnum S. R. 2000; HSP16.6 is involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium, Synechocystis sp. PCC 6803. Curr Microbiol 40:283–287
    [Google Scholar]
  15. Mamedov M., Hayashi H., Murata N. 1993; Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron-transport and phosphorylation reactions in S ynechocystis PCC6803. Biochim Biophys Acta 1142:1–5
    [Google Scholar]
  16. Masuda S., Ono T.-A. 2005; Adenylyl cyclase activity of Cya1 from the cyanobacterium Synechocystis sp. strain PCC 6803 is inhibited by bicarbonate. J Bacteriol 187:5032–5035
    [Google Scholar]
  17. Matsui M., Yoshimura T., Wakabayashi Y., Imamura I., Tanaka K., Takahashi H., Asayama M., Shirai M. 2007; Interference expression at levels of the transcript and protein among group 1, 2, and 3 sigma factor genes in a cyanobacterium. Microbes Environ 22:32–43
    [Google Scholar]
  18. Mi H., Endo T., Schreiber U., Ogawa T., Asada K. 1992; Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33:1233–1237
    [Google Scholar]
  19. Muro-Pastor A. M., Herrero A., Flores E. 2001a; Nitrogen-regulated group 2 sigma factor from Synechocystis sp. strain PCC 6803 involved in survival under nitrogen stress. J Bacteriol 183:1090–1095
    [Google Scholar]
  20. Muro-Pastor M. I., Reyes J. C., Florencio F. J. 2001b; Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276:38320–38328
    [Google Scholar]
  21. Nakamoto H., Suzuki M., Kojima K. 2003; Targeted inactivation of the hcrA repressor gene in cyanobacteria. FEBS Lett 549:57–62
    [Google Scholar]
  22. Nishiyama Y., Los D. A., Murata N. 1999; PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120:301–308
    [Google Scholar]
  23. Ogawa T., Kaplan A. 2003; Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77:105–115
    [Google Scholar]
  24. Osanai T., Kanesaki Y., Nakano T., Takahashi H., Asayama M., Shirai M., Kanehisa M., Suzuki I., Murata N., Tanaka K. 2005; Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 σ factor SigE. J Biol Chem 280:30653–30659
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Pollari M., Gunnelius L., Tuominen I., Ruotsalainen V., Tyystjärvi E., Salminen T., Tyystjärvi T. 2008; Characterization of single and double inactivation strains reveals new physiological roles for group 2 σ factors in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 147:1994–2005
    [Google Scholar]
  27. Pollari M., Ruotsalainen V., Rantamäki S., Tyystjärvi E., Tyystjärvi T. 2009; Simultaneous inactivation of sigma factors B and D interferes with light acclimation of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 191:3992–4001
    [Google Scholar]
  28. Singh A. K., Summerfield T. C., Li H., Sherman L. A. 2006; The heat shock response in the cyanobacterium Synechocystis sp. strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch Microbiol 186:273–286
    [Google Scholar]
  29. Slabas A. R., Suzuki I., Murata N., Simon W. J., Hall J. J. 2006; Proteomic analysis of the heat shock response in Synechocystis PCC6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics 6:845–864
    [Google Scholar]
  30. 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
    [Google Scholar]
  31. Terauchi K., Ohmori M. 1999; An adenylate cyclase, Cya1, regulates cell motility in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 40:248–251
    [Google Scholar]
  32. Tuominen I., Tyystjärvi E., Tyystjärvi T. 2003; Expression of primary sigma factor (PSF) and PSF-like sigma factors in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:1116–1119
    [Google Scholar]
  33. Tuominen I., Pollari M., Tyystjärvi E., Tyystjärvi T. 2006; The SigB sigma factor mediates high-temperature responses in the cyanobacterium Synechocystis sp. PCC6803. FEBS Lett 580:319–323
    [Google Scholar]
  34. Tuominen I., Pollari M., von Wobeser E. A., Tyystjärvi E., Ibelings B. W., Matthijs H. C. P., Tyystjärvi T. 2008; Sigma factor SigC is required for heat acclimation of the cyanobacterium Synechocystis sp. strain PCC 6803. FEBS Lett 582:346–350
    [Google Scholar]
  35. Tyystjärvi E., Vass I. 2004; Light emission as a probe of charge separation and recombination in the photosynthetic apparatus: relation of prompt fluorescence to delayed light emission and thermoluminescence. In Chlorophyll a Fluorescence: a Signature of Photosynthesis pp 363–388 Edited by Papageorgiou G. C. Govindjee Dordrecht: Springer;
    [Google Scholar]
  36. Vass I., Kirilovsky D., Etienne A.-L. 1999; UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp PCC 6803. Biochemistry 38:12786–12794
    [Google Scholar]
  37. 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
    [Google Scholar]
  38. Wösten M. M. S. M. 1998; Eubacterial sigma-factors. FEMS Microbiol Rev 22:127–150
    [Google Scholar]
  39. Xu M., Su Z. 2009; Computational prediction of cAMP receptor protein (CRP) binding sites in cyanobacterial genomes. BMC Genomics 10:23
    [Google Scholar]
  40. Xu M., Bernát G., Singh A., Mi H., Rögner M., Pakrasi H. B., Ogawa T. 2008; Properties of mutants of Synechocystis sp. strain PCC 6803 lacking inorganic carbon sequestration systems. Plant Cell Physiol 49:1672–1677
    [Google Scholar]
  41. Yeremenko N., Jeanjean R., Prommeenate P., Krasikov V., Nixon P. J., Vermaas W. F. J., Havaux M., Matthijs H. C. P. 2005; Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 46:1433–1436
    [Google Scholar]
  42. Yoshimura H., Yoshihara S., Okamoto S., Ikeuchi M., Ohmori M. 2002; A cAMP receptor protein, SYCRP1, is responsible for the cell motility of Synechocystis sp. PCC 6803. Plant Cell Physiol 43:460–463
    [Google Scholar]
  43. Zhang P., Battchikova N., Jansen T., Appel J., Ogawa T., Aro E.-M. 2004; Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocytis sp PCC 6803. Plant Cell 16:3326–3340
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032565-0
Loading
/content/journal/micro/10.1099/mic.0.032565-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error