Synthesis of fatty acids de novo is required for photosynthetic acclimation of Synechocystis sp. PCC 6803 to high temperature

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 8, 2010, Pages 1483-1490

  Nanjo, Yohei ^a   Mizusawa, Naoki ^b   Wada, Hajime ^b   Slabas, Antoni R ^c   Hayashi, Hidenori ^a   Nishiyama, Yoshitaka ^d  

^a EHIME UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c DURHAM UNIVERSITY   (United Kingdom)

^d SAITAMA UNIVERSITY   (Japan)

Author keywords

Acclimation; Fatty acid synthesis; High temperature stress; Photosystem II; Synechocystis; Thermotolerance

Indexed keywords

BACTERIAL PROTEIN; FATTY ACID; PROTEIN FABI; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; COLD ACCLIMATIZATION; CONTROLLED STUDY; FATTY ACID SYNTHESIS; GROWTH INHIBITION; HEAT TOLERANCE; HIGH TEMPERATURE; LIPID MEMBRANE; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SYNECHOCYSTIS; THERMOSTABILITY;

ACCLIMATIZATION; FATTY ACIDS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; SYNECHOCYSTIS; TEMPERATURE;

SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 77953809991     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.03.014     Document Type: Article

References (64)

1. Berry J., Björkman O. Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. 1980, 31:491-543.
2. Nash D., Miya M., Murata N. Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim. Biophys. Acta 1985, 807:127-133.
3. Thompson L.K., Blaylock R., Sturtevant J.M., Brudvig G.W. Molecular basis of the heat denaturation of photosystem II. Biochemistry 1989, 28:6686-6695.
4. Mamedov M., Hayashi H., Murata N. Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron-transport and phosphorylation reactions in Synechocystis sp. PCC6803. Biochim. Biophys. Acta 1993, 1142:1-5.
5. Nishiyama Y., Los D.A., Murata N. PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol. 1999, 120:301-308.
6. Kimura A., Eaton-Rye J.J., Morita E.H., Nishiyama Y., Hayashi H. Protection of the oxygen-evolving machinery by the extrinsic proteins of photosystem II is essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant Cell Physiol. 2002, 43:932-938.
7. Armond P.A., Schreiber U., Björkman O. Photosynthetic acclimation to temperature in the desert shrub, Larrea divaricata. II. Light-harvesting efficiency and electron transport. Plant Physiol. 1978, 61:411-415.
8. Pearcy R.W. Effects of growth temperature on the fatty acid composition of the leaf lipids in Atriplex lentiformis (Torr.) Wats. Plant Physiol. 1978, 61:484-486.
9. Raison J.K., Roberts J.K.M., Berry J.A. Correlation between the thermal stability of chloroplast (thylakoid) membranes and the composition and fluidity of their polar lipids upon acclimation of the higher plant Nerium oleander to growth temperature. Biochim. Biophys. Acta 1982, 688:218-228.
10. Nishiyama Y., Takechi K., Nanjo Y., Murata N., Hayashi H. Acclimation of photosystem II to high temperature in a suspension culture of soybean (Glycine max) requires proteins that are associated with the thylakoid membrane. Photosynth. Res. 2006, 90:223-232.
11. Fork D.C., Sen A., Williams W.P. The relationship between heat stress and photobleaching in green and blue algae. Photosynth. Res. 1987, 11:71-87.
12. Nishiyama Y., Kovacs E., Lee C.B., Hayashi H., Watanabe T., Murata N. Photosynthetic adaptation to high temperature associated with thylakoid membranes of Synechococcus PCC 7002. Plant Cell Physiol. 1993, 34:337-343.
13. Inoue N., Taira Y., Emi T., Yamane Y., Kashino Y., Koike H., Satoh K. Acclimation to the growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mesophilic cyanobacterium, Synechocystis sp. PCC 6803. Plant Cell Physiol. 2001, 42:1140-1148.
14. Tanaka Y., Nishiyama Y., Murata N. Acclimation of the photosynthetic machinery to high temperature in Chlamydomonas reinhardtii requires synthesis de novo of proteins encoded by the nuclear and chloroplast genomes. Plant Physiol. 2000, 124:441-449.
15. Thomas P.G., Dominy P.J., Vigh L., Mansourian A., Quinn P.J., Williams W.P. Increased thermal stability of pigment-protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. Biochim. Biophys. Acta 1986, 849:131-140.
16. Hugly S., Kunst L., Browse J., Somerville C. Enhanced thermal tolerance of photosynthesis and altered chloroplast ultrastructure in a mutant of Arabidopsis deficient in lipid desaturation. Plant Physiol. 1989, 90:1134-1142.
17. Sato N., Sonoike K., Kawaguchi A., Tsuzuki M. Contribution of lowered unsaturation levels of chloroplast lipids to high temperature tolerance of photosynthesis in Chlamydomonas reinhardtii. J. Photochem. Photobiol. 1996, 36:333-337.
18. Alfonso M., Yruela I., Almárcegui S., Torrado E., Pérez M.A., Picorel R. Unusual tolerance to high temperatures in a new herbicide-resistant D1 mutant from Glycine max (L.) Merr. Cell cultures deficient in fatty acid desaturation. Planta 2001, 212:573-582.
19. Aminaka R., Taira Y., Kashino Y., Koike H., Satoh K. Acclimation to the growth temperature and thermosensitivity of photosystem II in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant Cell Physiol. 2006, 47:1612-1621.
20. Gombos Z., Wada H., Murata N. Direct evaluation of effects of fatty-acid unsaturation on the thermal properties of photosynthetic activities, as studied by mutation and transformation of Synechocystis PCC6803. Plant Cell Physiol. 1991, 32:205-211.
21. Gombos Z., Wada H., Hideg E., Murata N. The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiol. 1994, 104:563-567.
22. Wada H., Gomboz Z., Murata N. Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:4273-4277.
23. Moon B.Y., Higashi S., Gombos Z., Murata N. Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:6215-6218.
24. Sato N., Aoki M., Maru Y., Sonoike K., Minoda A., Tsuzuki M. Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta 2003, 217:245-251.
25. Sakurai I., Mizusawa N., Ohashi S., Kobayashi M., Wada H. Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol. 2007, 144:1336-1346.
26. Sakurai I., Mizusawa N., Wada H., Sato N. Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol. 2007, 145:1361-1370.
27. Balogi Z., Török Z., Balogh G., Jósvay K., Shigapova N., Vierling E., Vígh L., Horváth I. "Heat shock lipid" in cyanobacteria during heat/light-acclimation. Arch. Biochem. Biophys. 2005, 436:346-354.
28. Mizusawa N., Sakata S., Sakurai I., Wada H. Involvement of digalactosyldiacylglycerol in cellular thermotolerance in Synechocystis sp. PCC 6803. Arch. Microbiol. 2009, 191:595-601.
29. Havaux M., Tardy F., Ravenel J., Chanu D., Parot P. Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content. Plant Cell Environ. 1996, 19:1359-1368.
30. Stapel D., Kruse E., Kloppstech K. The protective effect of heat shock protein against photoinhibition under heat shock in barley (Hordeum vulgare). J. Photochem. Photobiol. 1993, 21:211-218.
31. Eriksson M.J., Clarke A.K. The heat shock protein ClpB mediates the development of thermotolerance in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 1996, 178:4839-4846.
32. Heckathorn S.A., Downs C.A., Sharkey T.D., Coleman J.S. The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol. 1998, 116:439-444.
33. Nakamoto H., Suzuki N., Roy S.K. Constitutive expression of a small heat-shock protein confers cellular thermotolerance and thermal protection to the photosynthetic apparatus in cyanobacteria. FEBS Lett. 2000, 483:169-174.
34. Tsvetkova N.M., Horváth I., Török Z., Wolkers W.F., Balogi Z., Shigapova N., Crowe L.M., Tablin F., Vierling E., Crowe J.H., Vígh L. Small heat-shock proteins regulate membrane lipid polymorphism. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13504-13509.
35. Tuominen I., Pollari M., Tyystjärvi E., Tyystjärvi T. The SigB sigma factor mediates high-temperature responses in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 2006, 580:319-323.
36. Singh A.K., Summerfield T.C., Li H., Sherman L.A. The heat shock response in the cyanobacterium Synechocystis sp. strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch. Microbiol. 2006, 186:273-286.
37. Sharkey T.D., Singsaas E.L. Why plants emit isoprene. Nature 1995, 374:769.
38. Rock C.O., Cronan J.E. Escherichia coli as a model for the regulation of dissociable (type II) fatty acid biosynthesis. Biochim. Biophys. Acta 1996, 1302:1-16.
39. Egan A.F., Russell R.R.B. Conditional mutants affecting the cell envelope of Escherichia coli K-12. Genet. Res. Camb. 1973, 21:139-152.
40. Bergler H., Wallner P., Ebeling A., Leitinger B., Fuchsbichler S., Aschauer H., Kollenz G., Hogenauer G., Turnowsky F. Protein envM is the NADH-dependent enoyl-ACP reductase (FabI) of Escherichia coli. J. Biol. Chem. 1994, 269:5493-5496.
41. Heath R.J., Rock C.O. Enoyl-acyl carrier protein reductase (fabI) plays a determinant role in completing cycles of fatty acid elongation in Escherichia coli. J. Biol. Chem. 1995, 270:26538-26542.
42. Kaneko T., Sato S., Kotani H., Tanak A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S., Kimura T., Hosouchi T., Matsuno A., Muraki A., Nakazaki N., Naruo K., Okumura S., Shimpo S., Takeuchi C., Wada T., Watanabe A., Yamada M., Yasuda M., Tabata S. 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. 1996, 3:109-136.
43. Sakurai I., Shen J.R., Leng J., Ohashi S., Kobayashi M., Wada H. Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J. Biochem. 2006, 140:201-209.
44. Kashino Y., Koike H., Satoh K. An improved sodium dodecyl sulfate-polyacrylamide gel electrophoresis system for the analysis of membrane protein complexes. Electrophoresis 2001, 22:1004-1007.
45. Nishiyama Y., Yamamoto H., Allakhverdiev S.I., Inaba M., Yokota A., Murata N. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 2001, 20:5587-5594.
46. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37:911-917.
47. Wada H., Murata N. Synechocystis PCC 6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol. 1989, 30:971-978.
48. Levy C.W., Roujeiniikova A., Sedelnikova S., Baker P.J., Stuitje A.R., Slabas A.R., Rice D.W., Rafferty J.B. Molecular basis of triclosan activity. Nature 1999, 398:383-384.
49. Heath R.J., Rubin J.R., Holland D.R., Zhang E., Snow M.E., Rock C.O. Mechanism of triclosan inhibition of bacterial fatty acid synthesis. J. Biol. Chem. 1999, 274:11110-11114.
50. Slabas A.R., Smith C.G. Immunogold localisation of acylcarrier protein in plants and Escherichia coli: evidence for membrane association in plants. Planta 1980, 175:145-152.
51. 550 against heat inactivation in Synechococcus sp. PCC 7002. Plant Physiol. 1994, 105:1313-1319.
52. Nishiyama Y., Los D.A., Hayashi H., Murata N. Thermal protection of the oxygen-evolving machinery by PsbU, an extrinsic protein of photosystem II, in Synechococcus species PCC 7002. Plant Physiol. 1997, 115:1473-1480.
53. Wada H., Murata N. Temperature-induced changes in the fatty acid composition of the cyanobacterium Synechocystis PCC6803. Plant Physiol. 1990, 92:1062-1069.
54. Huang F., Parmryd I., Nilsson F., Persson A.L., Pakrasi H.B., Andersson B., Norling B. Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins. Mol. Cell Proteomics 2002, 1:956-966.
55. Nowaczyk M.M., Hebeler R., Schlodder E., Meyer H.E., Warscheid B., Rögner M. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 2006, 18:3121-3131.
56. Ujihara T., Sakurai I., Mizusawa N., Wada H. A method for analyzing lipid-modified proteins with mass spectrometry. Anal. Biochem. 2008, 374:429-431.
57. Wada H., Mizusawa N. The role of phosphatidylglycerol in photosynthesis. Lipids in Photosynthesis: Essential and Regulatory Functions 2009, 243-263. Springer, Dordrecht. H. Wada, N. Murata (Eds.).
58. Thornton L.E., Ohkawa H., Roose J.L., Kashino Y., Keren N., Pakrasi H.B. Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 2004, 16:2164-2175.
59. Roose J.L., Kashino Y., Pakrasi H.B. The PsbQ protein defines cyanobacterial photosystem II complexes with highest activity and stability. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2548-2553.
60. Roose J.L., Pakrasi H.B. The Psb27 protein facilitates manganese cluster assembly in photosystem II. J. Biol. Chem. 2008, 283:4044-4050.
61. Summerfield T.C., Shand J.A., Bentley F.K., Eaton-Rye J.J. PsbQ in Synechocystis sp. PCC6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions. Biochemistry 2005, 44:805-815.
62. Summerfield T.C., Winter R.T., Eaton-Rye J.J. Investigation of a requirement for the PsbP-like protein in Synechocystis sp. PCC6803. Photosynth. Res. 2005, 84:263-268.
63. Nishiyama Y., Allakhverdiev S.I., Murata N. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 2006, 1757:742-749.
64. Mulo P., Sirpiö S., Suorsa M., Aro E.-M. Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth. Res. 2008, 98:489-501.