Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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HspA and HtpG Enhance Thermotolerance in the Cyanobacterium, Microcystis aeruginosa NIES-298

  • Rhee, Jae-Sung (Department of Molecular and Environmental Bioscience, Graduate School, Hanyang University) ;
  • Ki, Jang-Seu (Department of Chemistry, College of Natural Sciences, Hanyang University) ;
  • Kim, Bo-Mi (Department of Chemistry, College of Natural Sciences, Hanyang University) ;
  • Hwang, Soon-Jin (Department of Environmental Science, College of Life and Environmental Science, Konkuk University) ;
  • Choi, Ik-Young (National Instrumentation Center for Environmental Management, Seoul National University) ;
  • Lee, Jae-Seong (Department of Molecular and Environmental Bioscience, Graduate School, Hanyang University)
  • Received : 2011.08.03
  • Accepted : 2011.09.08
  • Published : 2012.01.28
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Abstract

Heat shock proteins (Hsps) play a key role in the cellular defense response to diverse environmental stresses. Here, the role of Hsp genes in the acquisition of thermotolerance in the cyanobacterium Microcystis aeruginosa NIES-298 was investigated. Twelve Hsp-related genes were examined to observe their modulated expression patterns at different temperatures (10, 15, 25, and $35^{\circ}C$) over different exposure periods. HspA and HtpG transcripts showed an up-regulation of expression at low temperatures (10 and $15^{\circ}C$) and high temperature ($35^{\circ}C$), compared with the control ($25^{\circ}C$). To examine their effects upon thermotolerance, we purified recombinant HspA and HtpG proteins. During a thermotolerance study at $54^{\circ}C$, the HspA-transformed bacteria showed increased thermotolerance compared with the control. HtpG also played a role in the defense response to acute heat stress within 30 min. These findings provide a better understanding of cellular protection mechanisms against heat stress in cyanobacteria.

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References

  1. Bhagwat, A. A. and S. K. Apte. 1989. Comparative analysis of proteins induced by heat shock, salinity, and osmotic stress in the nitrogen-fixing cyanobacterium Anabaena sp. strain L-31. J. Bacteriol. 171: 5187-5189. https://doi.org/10.1128/jb.171.9.5187-5189.1989
  2. Blondin, P. A., R. J. Kirby, and S. R. Barnum. 1993. The heat shock response and acquired thermotolerance in three strains of cyanobacteria. Curr. Microbiol. 26: 79-84. https://doi.org/10.1007/BF01577340
  3. Borbély, G., G. Suranyi, A. Korcz, and Z. Palfi. 1985. Effect of heat shock on protein synthesis in the cyanobacterium Synechococcus sp. strain PCC 6301. J. Bacteriol. 161: 1125-1130.
  4. Chitnis, P. R. and N. Nelson. 1991. Molecular cloning of the genes encoding two chaperone proteins of the cyanobacterium Synechocystis sp. PCC 680. J. Biol. Chem. 266: 58-65.
  5. Crack, J. A., M. Mansour, Y. Sun, and T. H. MacRae. 2002. Functional analysis of a small heat shock/-crystallin protein from Artemia franciscana; oligomerization and thermotolerance. Eur. J. Biochem. 269: 933-942. https://doi.org/10.1046/j.0014-2956.2001.02726.x
  6. de Figueiredo, D. R., A. S. S. P. Reboleira, S. C. Antunes, N. Abrantes, U. Azeiteiro, F. Gonçalves, and M. J. Pereria. 2006. The effect of environmental parameters and cyanobacterial blooms on phytoplankton dynamics of a Portuguese temperate lake. Hydrobiologia 568: 145-157. https://doi.org/10.1007/s10750-006-0196-y
  7. Fang, F. and S. R. Barnum. 2003. The heat shock gene, htpG, and thermotolerance in the cyanobacterium, Synechocystis sp. PCC 6803. Curr. Microbiol. 47: 341-346. https://doi.org/10.1007/s00284-002-4015-z
  8. Feder, M. E. and G. E. Hofmann. 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61: 243-282. https://doi.org/10.1146/annurev.physiol.61.1.243
  9. Giese, K. C. and E. Vierling. 2004. Mutants in small heat shock proteins that affect the oligomeric state: Analysis and allele specific suppression. J. Biol. Chem. 279: 32674-32683. https://doi.org/10.1074/jbc.M404455200
  10. Hossain, M. M. and H. Nakamoto. 2002. HtpG plays a role in cold acclimation in cyanobacteria. Curr. Microbiol. 44: 291-296. https://doi.org/10.1007/s00284-001-0005-9
  11. Kanoshina, I., U. Lipsb, and J. M. Leppanen. 2003. The influence of weather conditions (temperature and wind) on cyanobacterial bloom development in the Gulf of Finland (Baltic Sea). Harmful Algae 2: 29-41. https://doi.org/10.1016/S1568-9883(02)00085-9
  12. Kojima, K. and H. Nakamoto. 2005. Post-transcriptional control of the cyanobacterial hspA heat-shock induction. Biochem. Biophys. Res. Commun. 3: 583-588.
  13. Lee, S., D. J. Prochaska, F. Fang, and S. R. Barnum. 1998. A 16.6-kilodalton protein in the cyanobacterium Synechocystis sp. PCC 6803 plays a role in the heat shock response. Curr. Microbiol. 37: 403-407. https://doi.org/10.1007/s002849900400
  14. Lehel, C., H. Wada, E. Kovacs, Z. Torok, Z. Gombos, I. Horvath, et al. 1992. Heat shock protein synthesis of the cyanobacterium Synechocystis PCC 6803: Purification of the GroEL-related chaperonin. Plant Mol. Biol. 18: 327-336. https://doi.org/10.1007/BF00034959
  15. Leroux, M. R., R. Melki, B. Gordon, G. Batelier, and E. P. M. Candido. 1997. Structure-function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides. J. Biol. Chem. 272: 24646-24656. https://doi.org/10.1074/jbc.272.39.24646
  16. Livak, K. J. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real time quantitative PCR and the $2^{-{\Delta}{\Delta}C}$ method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  17. Muchowski, P. J., G. J. S. Wu, J. J. N. Liang, E. T. Adman, and J. I. Clark. 1999. Site-directed mutations within the core '$\alpha$-crystallin' domain of the small heat shock protein, human ${\alpha}{\beta}$-crystallin, decrease molecular chaperone functions. J. Mol. Biol. 289: 397-411. https://doi.org/10.1006/jmbi.1999.2759
  18. Nakamoto, H., N. Suzuki, and S. K. Roy. 2000. Constitutive expression of a small heat-shock protein confers cellular thermotolerance and thermal protection to the photosynthetic apparatus in cyanobacteria. FEBS Lett. 20: 169-174.
  19. Nimura, K., H. Takahashi, and H. Yoshikawa. 2001. Characterization of the dnaK multigene family in the cyanobacterium Synechococcus sp. strain PCC7942. J. Bacteriol. 183: 1320-1328. https://doi.org/10.1128/JB.183.4.1320-1328.2001
  20. Parcellier, A., S. Gurbuxani, E. Schmitt, E. Solary, and C. Garrido. 2003. Heat shock proteins, cellular chaperones that modulate mitochondrial cell death pathways. Biochem. Biophys. Res. Commun. 304: 505-512. https://doi.org/10.1016/S0006-291X(03)00623-5
  21. Picard, D. 2002. Heat-shock protein 90, a chaperone for folding and regulation. Cell. Mol. Life Sci. 59: 1640-1648. https://doi.org/10.1007/PL00012491
  22. Rajaram, H., A. D. Ballal, S. K. Apte, T. Wiegert, and W. Schumann. 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. https://doi.org/10.1016/S0167-4781(01)00222-6
  23. Rhee, J.-S., S. Raisuddin, K.-W. Lee, J.-S. Seo, J.-S. Ki, I.-C. Kim, et al. 2008. Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp. Biochem. Physiol C 149: 104-112.
  24. Robarts, R. D. and T. Zohary. 1987. Temperature effects on photosynthetic capacity, respiration, and growth rates of bloomforming cyanobacteria. N.Z.J. Mar. Freshwater Res. 21: 391-399. https://doi.org/10.1080/00288330.1987.9516235
  25. Roy, S. K., T. Hiyama, and H. Nakamoto. 1999. Purification and characterization of the 16-kDa heat-shock-responsive protein from the thermophilic cyanobacterium Synechococcus vulcanus, which is an alpha-crystallin-related, small heat shock protein. Eur. J. Biochem. 262: 406-416. https://doi.org/10.1046/j.1432-1327.1999.00380.x
  26. Seo, J.-S., Y.-M. Lee, H.-G. Park, and J.-S. Lee. 2006. The intertidal copepod Tigriopus japonicus small heat shock protein 20 gene Hsp20 enhances thermotolerance of transformed Escherichia coli. Biochem. Biophys. Res. Commun. 340: 901-908. https://doi.org/10.1016/j.bbrc.2005.12.086
  27. Suzuki, I., Y. Kanesaki, H. Hayashi, J. J. Hall, W. J. Simon, A. R. Slabas, and N. Murata. 2005. The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis. Plant Physiol. 138: 1409-1421. https://doi.org/10.1104/pp.104.059097
  28. Tanaka, N. and H. Nakamoto. 1999. HtpG is essential for the thermal stress management in cyanobacteria. FEBS Lett. 17: 117-123.
  29. van Montfort, R., C. Slingsby, and E. Vierling. 2002. Structure and function of the small heat shock protein/$\alpha$-crystallin family of molecular chaperones. Adv. Prot. Chem. 59: 105-156.
  30. Yura, T. and K. Nakahigashi. 1999. Regulation of the heatshock response. Curr. Opin. Microbiol. 2: 153-158. https://doi.org/10.1016/S1369-5274(99)80027-7
  31. Horwitz, J. 1992. $\alpha$-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89: 10449-10453. https://doi.org/10.1073/pnas.89.21.10449
  32. Thomas, J. G. and F. Baneyx. 1996. Protein misfolding and inclusion body formation in recombinant Escherichia coli cells overexpressing heat-shock proteins. J. Biol. Chem. 10: 11141-11147.

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