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Proteomic analysis of Synechocystis sp. PCC6803 responses to low-temperature and high light conditions

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Abstract

The global changes in protein expression of Synechocystis sp. PCC6803, a photosynthetic bacterium for the production of secondary metabolites as a green cell factory, were investigated by proteome separation and a subsequent tandem mass spectrometry. Two different proteome separation techniques, strong cation exchange chromatography and off-gel electrophoresis, were applied. The combination of the two proteome separation techniques enabled the comparative analysis of the differential regulation of the Synechocystis proteome in response to two different environmental factors, temperature and light. A total of 1,483 proteins were identified, which represent over 40% of the genes in Synechocystis. Our data showed that fatty acid metabolism was inhibited by (3R)-hydroxymyristol acyl carrier protein dehydrase (Sll1605) under low temperature conditions. The expression of UDP-N-acetylglucosamine acyltransferase (Sll0379) and 3-O-[3-hydroxymyristoyl] glucosamine N-acyltransferase (Slr0776), which is involved in lipopolysaccharide metabolism, was not observed under high light conditions. Under high light exposure, proteins related to iron-sulfur metabolism were detected, which may be responsible for maintaining the redox potential of the photosystem. High light under low temperature caused severe damage to the photosystem. Some of the responses to these stresses were similar to those previously reported for other photosynthetic organisms. Notably, this study revealed the followings: (i) low temperature inhibits fatty acid synthesis; (ii) high light inhibits lipopolysaccharides synthesis and stimulates the expression of iron-sulfur related proteins; and (iii) high light under low temperature induces the photorespiratory cycle. The global proteomic analysis clearly showed that stress conditions such as low temperature and/or high light induce cellular metabolisms related with the protection of their photosystems in the model microalga Synechocystis sp. PCC6803.

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References

  1. Burja, A. M., S. Dhamwichukorn, and P. C. Wright (2003) Cyanobacterial postgenomic research and systems biology. Trends Biotechnol. 21: 504–511.

    Article  CAS  Google Scholar 

  2. Suzuki, I., Y. Kanesaki, K. Mikami, M. Kanehisa, and N. Murata (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol. Microbiol. 40: 235–244.

    Article  CAS  Google Scholar 

  3. Gill, R. T., E. Katsoulakis, W. Schmitt, G. Taroncher-Oldenburg, J. Misra, and G. Stephanopoulos (2002) Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. J. Bacteriol. 184: 3671–3681.

    Article  CAS  Google Scholar 

  4. Hihara, Y., A. Kamei, M. Kanehisa, A. Kaplan, and M. Ikeuchi (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13: 793–806.

    Article  CAS  Google Scholar 

  5. Hihara, Y., K. Sonoike, M. Kanehisa, and M. Ikeuchi (2003) DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 185: 1719–1725.

    Article  CAS  Google Scholar 

  6. Osanai, T., S. Imamura, M. Asayama, M. Shirai, I. Suzuki, N. Murata, and K. Tanaka (2006) Nitrogen induction of sugar catabolic gene expression in Synechocystis sp. PCC 6803. DNA Res. 13: 185–195.

    Article  CAS  Google Scholar 

  7. Osanai, T., Y. Kanesaki, T. Nakano, H. Takahashi, M. Asayama, M. Shirai, M. Kanehisa, I. Suzuki, N. Murata, and K. Tanaka (2005) Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 sigma factor sigE. J. Biol. Chem. 280: 30653–30659.

    Article  CAS  Google Scholar 

  8. Schmitt, W. A. Jr. and G. Stephanopoulos (2003) Prediction of transcriptional profiles of Synechocystis PCC6803 by dynamic autoregressive modeling of DNA microarray data. Biotechnol. Bioeng. 84: 855–863.

    Article  CAS  Google Scholar 

  9. Ohkawa, H., M. Sonoda, M. Shibata, and T. Ogawa (2001) Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 183: 4938–4939.

    Article  CAS  Google Scholar 

  10. Herranen, M., N. Battchikova, P. Zhang, A. Graf, S. Sirpio, V. Paakkarinen, and E. M. Aro (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol. 134: 470–481.

    Article  CAS  Google Scholar 

  11. Huang, F., E. Hedman, C. Funk, T. Kieselbach, W. P. Schroder, and B. Norling (2004) Isolation of outer membrane of Synechocystis sp. PCC 6803 and its proteomic characterization. Mol. Cell Proteom. 3: 586–595.

    Article  CAS  Google Scholar 

  12. Huang, F., I. Parmryd, F. Nilsson, A. L. Persson, H. B. Pakrasi, B. Andersson, and B. Norling (2002) Proteomics of Synechocystis sp. strain PCC 6803: Identification of plasma membrane proteins. Mol. Cell Proteom. 1: 956–966.

    Article  CAS  Google Scholar 

  13. Pisareva, T., M. Shumskaya, G. Maddalo, L. Ilag, and B. Norling (2007) Proteomics of Synechocystis sp. PCC 6803. Identification of novel integral plasma membrane proteins. FEBS J. 274: 791–804.

    Article  CAS  Google Scholar 

  14. Rajalahti, T., F. Huang, M. R. Klement, T. Pisareva, M. Edman, M. Sjostrom, A. Wieslander, and B. Norling (2007) Proteins in different Synechocystis compartments have distinguishing N-terminal features: A combined proteomics and multivariate sequence analysis. J. Proteome Res. 6: 2420–2434.

    Article  CAS  Google Scholar 

  15. Battchikova, N., J. P. Vainonen, N. Vorontsova, M. Keranen, D. Carmel, and E. M. Aro (2010) Dynamic changes in the proteome of Synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics. J. Proteome Res. 9: 5896–5912.

    Article  CAS  Google Scholar 

  16. Liu, J., L. Chen, J. Wang, J. Qiao, and W. Zhang (2012) Proteomic analysis reveals resistance mechanism against biofuel hexane in Synechocystis sp. PCC 6803. Biotechnol. Biofuels 5: 68.

    Article  CAS  Google Scholar 

  17. Wegener, K. M., A. K. Singh, J. M. Jacobs, T. Elvitigala, E. A. Welsh, N. Keren, M. A. Gritsenko, B. K. Ghosh, D. G. Camp, R. D. Smith, and H. B. Pakrasi (2010) Global proteomics reveal an atypical strategy for carbon/nitrogen assimilation by a cyanobacterium under diverse environmental perturbations. Mol. Cell Proteom. 9: 2678–2689.

    Article  CAS  Google Scholar 

  18. Bhandari, R. and P. K. Sharma (2006) High-light-induced changes on photosynthesis, pigments, sugars, lipids and antioxidant enzymes in freshwater (Nostoc spongiaeforme) and marine (Phormidium corium) cyanobacteria. Photochem. Photobiol. 82: 702–710.

    Article  CAS  Google Scholar 

  19. Sakamoto, T. and N. Murata (2002) Regulation of the desaturation of fatty acids and its role in tolerance to cold and salt stress. Curr. Opin. Microbiol. 5: 206–210.

    Article  CAS  Google Scholar 

  20. Inaba, M., I. Suzuki, B. Szalontai, Y. Kanesaki, D. A. Los, H. Hayashi, and N. Murata (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J. Biol. Chem. 278: 12191–12198.

    Article  CAS  Google Scholar 

  21. Hihara, Y., K. Sonoike, and M. Ikeuchi (1998) A novel gene, pmgA, specifically regulates photosystem stoichiometry in the cyanobacterium Synechocystis species PCC 6803 in response to high light. Plant Physiol. 117: 1205–1216.

    Article  CAS  Google Scholar 

  22. Sheng, J., H. W. Kim, J. P. Badalamenti, C. Zhou, S. Sridharakrishnan, R. Krajmalnik-Brown, B. E. Rittmann, and R. Vannela (2011) Effects of temperature shifts on growth rate and lipid characteristics of Synechocystis sp. PCC6803 in a bench-top photobioreactor. Bioresour. Technol. 102: 11218–11225.

    Article  CAS  Google Scholar 

  23. Gigova, L., G. Gacheva, N. Ivanova, and P. Pilarski (2012) Effets of temperature on Synechocystis sp. R10 (cyanoprokaryota) at two irradiance levels. I. Effect on growth, biochemical composition and defense enzyme activities. Genet. Plant Physiol. 2: 24–37.

    Google Scholar 

  24. Boussiba, S. (2000) Carotenogenesis in the green alga Haematococcus pluvialis: Cellular physiology and stress response. Physiol. Plant 108: 111–117.

    Article  CAS  Google Scholar 

  25. Reed, R. H., D. L. Richardson, S. R. C. Warr, and W. D. P. Stewart (1984) Carbohydrate accumulation and osmotic stress in cyanobacteria. J. Gen. Microbiol. 130: 1–4.

    CAS  Google Scholar 

  26. Takagi, M., Karseno, and T. Yoshida (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J. Biosci. Bioeng. 101: 223–226.

    Article  CAS  Google Scholar 

  27. Kim, D. K., S. J. Hong, J. H. Bae, N. Yim, E. Jin, and C. G. Lee (2011) Transcriptomic analysis of Haematococcus lacustris during astaxanthin accumulation under high irradiance and nutrient starvation. Biotechnol. Bioproc. Eng. 16: 698–705.

    Article  CAS  Google Scholar 

  28. Tran, N. P., J. K. Park, Z. H. Kim, and C. G. Lee (2009) Influence of sodium orthovanadate on the production of astaxanthin from green algae Haematococcus lacustris. Biotechnol. Bioproc. Eng. 14: 322–329.

    Article  CAS  Google Scholar 

  29. Schenk, P., S. Thomas-Hall, E. Stephens, U. Marx, J. Mussgnug, C. Posten, O. Kruse, and B. Hankamer (2008) Second generation biofuels: High-efficiency microalgae for biodiesel production. BioEnergy Res. 1: 20–43.

    Article  Google Scholar 

  30. Tran, H. L., Y. J. Ryu, D. H. Seong, S. M. Lim, and C. G. Lee (2013) An effective acid catalyst for biodiesel production from impure raw feedstocks. Biotechnol. Bioproc. Eng. 18: 242–247.

    Article  CAS  Google Scholar 

  31. Mironov, K. S., R. A. Sidorov, M. S. Trofimova, V. S. Bedbenov, V. D. Tsydendambaev, S. I. Allakhverdiev, and D. A. Los (2012) Light-dependent cold-induced fatty acid unsaturation, changes in membrane fluidity, and alterations in gene expression in Synechocystis. Biochim. Biophys. Acta 1817: 1352–1359.

    Article  CAS  Google Scholar 

  32. Los, D. A., A. Zorina, M. Sinetova, S. Kryazhov, K. Mironov, and V. V. Zinchenko (2010) Stress sensors and signal transducers in cyanobacteria. Sensors (Basel) 10: 2386–2415.

    Article  CAS  Google Scholar 

  33. Jeamton, W., S. Mungpakdee, M. Sirijuntarut, P. Prommeenate, S. Cheevadhanarak, M. Tanticharoen, and A. Hongsthong (2008) A combined stress response analysis of Spirulina platensis in terms of global differentially expressed proteins, and mRNA levels and stability of fatty acid biosynthesis genes. FEMS Microbiol. Lett. 281: 121–131.

    Article  CAS  Google Scholar 

  34. Sato, N. and N. Murata (1981) Studies on the temperature shiftinduced desaturation of fatty acids in monogalactosyl diacylglycerol in the blue-green alga (Cyanobacterium), Anabaena variabilis. Plant Cell Physiol. 22: 1043–1050.

    CAS  Google Scholar 

  35. Wada, H. and N. Murata (1990) Temperature-induced changes in the fatty acid composition of the cyanobacterium, Synechocystis PCC6803. Plant Physiol. 92: 1062–1069.

    Article  CAS  Google Scholar 

  36. Szklarczyk, D., A. Franceschini, M. Kuhn, M. Simonovic, A. Roth, P. Minguez, T. Doerks, M. Stark, J. Muller, P. Bork, L. J. Jensen, and C. Von Mering (2011) The STRING database in 2011: Functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39: 561–568.

    Article  Google Scholar 

  37. Katoh, H., N. Hagino, A. R. Grossman, and T. Ogawa (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 183: 2779–2784.

    Article  CAS  Google Scholar 

  38. Zhang, Z., N. D. Pendse, K. N. Phillips, J. B. Cotner, and A. Khodursky (2008) Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genom. 9: 344.

    Article  Google Scholar 

  39. Asada, K. (1994) Production and action of active oxygen species in photosynthetic tissues. pp. 77–104. In: Foyer, C. H. and P. M. Mullineaux (eds.). Causes of Photooxidative stress and Amelioration of Defense Systems in Plants. CRC Press.

    Google Scholar 

  40. Cooley, J. W., C. A. Howitt, and W. F. Vermaas (2000) Succinate: quinol oxidoreductases in the cyanobacterium Synechocystis sp. strain PCC 6803: Presence and function in metabolism and electron transport. J. Bacteriol. 182: 714–722.

    Article  CAS  Google Scholar 

  41. Silva, P., Y. J. Choi, H. A. Hassan, and P. J. Nixon (2002) Involvement of the HtrA family of proteases in the protection of the cyanobacterium Synechocystis PCC 6803 from light stress and in the repair of photosystem II. Philos. Trans. R Soc. Lond. B Biol. Sci. 357: 1461–1467.

    Article  CAS  Google Scholar 

  42. Allakhverdiev, S. I. and N. Murata (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta-Bioenerg 1657: 23–32.

    Article  CAS  Google Scholar 

  43. Gombos, Z., H. Wada, and N. Murata (1992) Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC6803 to low-temperature photoinhibition. Proc. Natl. Acad. Sci. U. S. A. 89: 9959–9963.

    Article  CAS  Google Scholar 

  44. Taylor, A. O. and J. A. Rowley (1971) Plants under climatic stress: I. Low temperature, high light effects on photosynthesis. Plant Physiol. 47: 713–718.

    Article  CAS  Google Scholar 

  45. Aro, E. M., I. Virgin, and B. Andersson (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143: 113–134.

    Article  CAS  Google Scholar 

  46. Barker, M., R. De Vries, J. Nield, J. Komenda, and P. J. Nixon (2006) The Deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J. Biol. Chem. 281: 30347–30355.

    Article  CAS  Google Scholar 

  47. Appel, J., S. Phunpruch, K. Steinmuller, and R. Schulz (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch. Microbiol. 173: 333–338.

    Article  CAS  Google Scholar 

  48. Schmitz, O., G. Boison, H. Salzmann, H. Bothe, K. Schutz, S. H. Wang, and T. Happe (2002) HoxE — a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim. Biophys. Acta-Bioenerg 1554: 66–74.

    Article  CAS  Google Scholar 

  49. Singh, A. K. and L. A. Sherman (2005) Pleiotropic effect of a histidine kinase on carbohydrate metabolism in Synechocystis sp. strain PCC 6803 and its requirement for heterotrophic growth. J. Bacteriol. 187: 2368–2376.

    Article  CAS  Google Scholar 

  50. Eisenhut, M., S. Kahlon, D. Hasse, R. Ewald, J. Lieman-Hurwitz, T. Ogawa, W. Ruth, H. Bauwe, A. Kaplan, and M. Hagemann (2006) The plant-like C2 glycolate cycle and the bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiol. 142: 333–342.

    Article  CAS  Google Scholar 

  51. Takahashi, S., H. Bauwe, and M. Badger (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol. 144: 487–494.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Marine Bioenergy Research Center, Department of Biological Engineering, Inha University, Incheon, 402-751, Korea

    Seong-Joo Hong, Jin Hee Jang & Choul-Gyun Lee

  2. Institute of Pharmaceutical Research, College of Pharmacy, Gachon University, Incheon, 406-840, Korea

    HyoJin Kim & Hookeun Lee

  3. Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon, 305-701, Korea

    Byung-Kwan Cho

  4. College of Pharmacy, Chung-Ang University, Seoul, 156-756, Korea

    Hyung-Kyoon Choi

  5. Gachon Medical Research Institute, Gil Medical Center, Incheon, 405-760, Korea

    Hookeun Lee

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  1. Seong-Joo Hong
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Hong, SJ., Kim, H., Jang, J.H. et al. Proteomic analysis of Synechocystis sp. PCC6803 responses to low-temperature and high light conditions. Biotechnol Bioproc E 19, 629–640 (2014). https://doi.org/10.1007/s12257-013-0563-2

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