1887

Abstract

Cyanobacteria constitute an ancient, diverse and ecologically important bacterial group. The responses of these organisms to light and nutrient conditions are finely controlled, enabling the cells to survive a range of environmental conditions. In particular, it is important to understand how cyanobacteria acclimate to the absorption of excess excitation energy and how stress-associated transcripts accumulate following transfer of cells from low- to high-intensity light. In this study, quantitative RT-PCR was used to monitor changes in levels of transcripts encoding chaperones and stress-associated proteases in three cyanobacterial strains that inhabit different ecological niches: the freshwater strain sp. PCC 6803, the marine high-light-adapted strain MED4 and the marine low-light-adapted strain MIT9313. Levels of transcripts encoding stress-associated proteins were very sensitive to changes in light intensity in all of these organisms, although there were significant differences in the degree and kinetics of transcript accumulation. A specific set of genes that seemed to be associated with high-light adaptation (/, , , and ) could be targeted for more detailed studies in the future. Furthermore, the strongest responses were observed in MED4, a strain characteristic of the open ocean surface layer, where genes could play a critical role in cell survival.

Keyword(s): HL, high light and LL, low light
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/content/journal/micro/10.1099/mic.0.27014-0
2004-05-01
2021-05-05
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References

  1. Apte S. K., Fernandes T., Badran H., Ballal A. 1998; Expression and possible role of stress-responsive proteins in Anabaena. J Biosci 23:399–406 [CrossRef]
    [Google Scholar]
  2. Asada K. 1994; Production and action of active oxygen species in photosynthetic tissues. In Causes of Photooxidative Stress and Amelioration of Defence Systems in Plants pp. 77–104Edited by Foyer C. H., Mullineaux P. M. Boca Raton, FL: CRC Press;
    [Google Scholar]
  3. Bhaya D., Vaulot D., Amin P., Takahashi A., Grossman A. 2000; Isolation of regulated genes of the cyanobacterium Synechocystis sp. strain PCC 6803 by differential display. J Bacteriol 182:5692–5699 [CrossRef]
    [Google Scholar]
  4. Bhaya D., Dufresne A., Vaulot D., Grossman A. 2002; Analysis of the hli gene family in marine and freshwater cyanobacteria. FEMS Microbiol Lett 215:209–219 [CrossRef]
    [Google Scholar]
  5. Bukau B., Horwich A. L. 1998; The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366 [CrossRef]
    [Google Scholar]
  6. Clarke A. K., Eriksson M. J. 1996; The cyanobacterium Synechococcus sp. PCC 7942 possesses a close homologue to the chloroplast ClpC protein of higher plants. Plant Mol Biol 31:721–730 [CrossRef]
    [Google Scholar]
  7. Clarke A. K., Schelin J., Porankiewicz J. 1998; Inactivation of the clpP1 gene for the proteolytic subunit of the ATP-dependent Clp protease in the cyanobacterium Synechococcus limits growth and light acclimation. Plant Mol Biol 37:791–801 [CrossRef]
    [Google Scholar]
  8. De Saizieu A., Certa U., Warrington J., Gray C., Keck W., Mous J. 1998; Bacterial transcript imaging by hybridization of total RNA to oligonucleotide arrays. Nat Biotechnol 16:45–48
    [Google Scholar]
  9. Eriksson M. J., Clarke A. K. 1996; The heat shock protein ClpB mediates the development of thermotolerance in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 178:4839–4846
    [Google Scholar]
  10. Eriksson M. J., Schelin J., Miskiewicz E., Clarke A. K. 2001; Novel form of ClpB/HSP100 protein in the cyanobacterium Synechococcus. J Bacteriol 183:7392–7396 [CrossRef]
    [Google Scholar]
  11. Glatz A., Horvath I., Varvasovszki V., Kovacs E., Torok Z., Vigh L. 1997; Chaperonin genes of the Synechocystis PCC 6803 are differentially regulated under light-dark transition during heat stress. Biochem Biophys Res Commun 239:291–297 [CrossRef]
    [Google Scholar]
  12. Glatz A., Vass I., Los D. A., Vigh L. 1999; The Synechocystis model of stress: from molecular chaperones to membranes. Plant Physiol Biochem 37:1–12 [CrossRef]
    [Google Scholar]
  13. Glover J. R., Lindquist S. 1998; Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94:73–82 [CrossRef]
    [Google Scholar]
  14. Gottesman S. 1996; Proteases and their targets in Escherichia coli. Annu Rev Genet 30:465–506 [CrossRef]
    [Google Scholar]
  15. Gottesman S., Wickner S., Maurizi M. R. 1997; Protein quality control: triage by chaperones and proteases. Genes Dev 11:815–823 [CrossRef]
    [Google Scholar]
  16. Gottesman S., Roche E., Zhou Y., Sauer R. T. 1998; The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12:1338–1347 [CrossRef]
    [Google Scholar]
  17. He Q., Dolganov N., Bjorkman O., Grossman A. R. 2001; The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276:306–314 [CrossRef]
    [Google Scholar]
  18. Herman C., D'Ari R. 1998; Proteolysis and chaperones: the destruction/reconstruction dilemma. Curr Opin Microbiol 1:204–209 [CrossRef]
    [Google Scholar]
  19. 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]
    [Google Scholar]
  20. Hossain M. M., Nakamoto H. 2002; HtpG plays a role in cold acclimation in cyanobacteria. Curr Microbiol 44:291–296 [CrossRef]
    [Google Scholar]
  21. Hossain M. M., Nakamoto H. 2003; Role for the cyanobacterial HtpG in protection from oxidative stress. Curr Microbiol 46:70–76 [CrossRef]
    [Google Scholar]
  22. 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 [CrossRef]
    [Google Scholar]
  23. Jacquet S., Partensky F., Marie D., Casotti R., Vaulot D. 2001; Cell cycle regulation by light in Prochlorococcus strains. Appl Environ Microb 67:782–790 [CrossRef]
    [Google Scholar]
  24. Kaneko T., Sato S., Kotani H.21 other authors 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystissp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136 [CrossRef]
    [Google Scholar]
  25. Kovacs E., van der Vies S. M., Glatz A., Torok Z., Varvasovszki V., Horvath I., Vigh L. 2001; The chaperonins of Synechocystis PCC 6803 differ in heat inducibility and chaperone activity. Biochem Biophys Res Commun 289:908–915 [CrossRef]
    [Google Scholar]
  26. Levchenko I., Luo L., Baker T. 1995; Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 9:2399–2408 [CrossRef]
    [Google Scholar]
  27. Lindquist S., Craig E. A. 1988; The heat-shock proteins. Annu Rev Genet 22:631–677 [CrossRef]
    [Google Scholar]
  28. Mann N. H. 2002; Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol Lett 27:17–34
    [Google Scholar]
  29. Mary I., Vaulot D. 2003; Two-component systems in Prochlorococcus MED4: genomic analysis and differential expression under stress. FEMS Microbiol Lett 226:135–144 [CrossRef]
    [Google Scholar]
  30. Moore L. R., Goericke R., Chisholm S. W. 1995; Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar Ecol Prog Ser 116:259–275 [CrossRef]
    [Google Scholar]
  31. Moore L. R., Rocap G., Chisholm S. W. 1998; Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393:464–467 [CrossRef]
    [Google Scholar]
  32. Moore L. R., Post A. F., Rocap G., Chisholm S. W. 2002; Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47:989–96 [CrossRef]
    [Google Scholar]
  33. Nimura K., Takahashi H., Yoshikawa H. 2001; Characterization of the dnaK multigene family in the cyanobacteriumSynechococcus sp. strain PCC7942. . J Bacteriol 183:1320–1328 [CrossRef]
    [Google Scholar]
  34. Partensky F., Hess W. R., Vaulot D. 1999; Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127
    [Google Scholar]
  35. Porankiewicz J., Clarke A. K. 1997; Induction of the heat shock protein ClpB affects cold acclimation in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 179:5111–5117
    [Google Scholar]
  36. Porankiewicz J., Schelin J., Clarke A. K. 1998; The ATP-dependent Clp protease is essential for acclimation to UV-B and low temperature in the cyanobacterium Synechococcus. Mol Microbiol 29:275–283 [CrossRef]
    [Google Scholar]
  37. Porankiewicz J., Wang J., Clarke A. 1999; New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32:449–458 [CrossRef]
    [Google Scholar]
  38. Queitsch C., Hong S. W., Vierling E., Lindquist S. 2000; Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492 [CrossRef]
    [Google Scholar]
  39. Rajaram H., Ballal A. D., Apte S. K., Wiegert T., Schumann W. 2001; Cloning and characterization of the major groESL operon from a nitrogen-fixing cyanobacterium,Anabaena sp. strain L-31. Biochim Biophys Acta 1519:143–146 [CrossRef]
    [Google Scholar]
  40. 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]
  41. Rocap G., Larimer F. W., Lamerdin J.21 other authors 2003; Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1001–1002 [CrossRef]
    [Google Scholar]
  42. Schelin J., Lindmark F., Clarke A. K. 2002; The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiology 148:2255–2265
    [Google Scholar]
  43. Tanaka N., Nakamoto H. 1999; HtpG is essential for the thermal stress management in cyanobacteria. FEBS Lett 458:117–123 [CrossRef]
    [Google Scholar]
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