Abstract
The cyanobacterium Synechococcus sp. strain PCC 7942 was transformed with the codA gene for choline oxidase from Arthrobacter globiformis under the control of a constitutive promoter. This transformation allowed the cyanobacterial cells to accumulate glycine betaine at 60 to 80 mM in the cytoplasm. The transformed cells could grow at 20 degrees C, the temperature at which the growth of control cells was markedly suppressed. Photosynthesis of the transformed cells at 20 degrees C was more tolerant to light than that of the control cells. This was caused by the enhanced ability of the photosynthetic machinery in the transformed cells to recover from low-temperature photoinhibition. In darkness, photosynthesis of the transformed cells was more tolerant to low temperature such as 0 to 10 degrees C than that of the control cells. In parallel with the improvement in the ability of the transformed cells to tolerate low temperature, the lipid phase transition of plasma membranes from the liquid-crystalline state to the gel state shifted toward lower temperatures, although the level of unsaturation of the membrane lipids was unaffected by the transformation. These findings suggest that glycine betaine enhances the tolerance of photosynthesis to low temperature.
Full Text
The Full Text of this article is available as a PDF (225.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aro E. M., Virgin I., Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993 Jul 5;1143(2):113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
- BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
- Brand J. J. Spectral Changes in Anacystis nidulans Induced by Chilling. Plant Physiol. 1977 May;59(5):970–973. doi: 10.1104/pp.59.5.970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deshnium P., Los D. A., Hayashi H., Mustardy L., Murata N. Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol. 1995 Dec;29(5):897–907. doi: 10.1007/BF00014964. [DOI] [PubMed] [Google Scholar]
- Garcia-Perez A., Burg M. B. Renal medullary organic osmolytes. Physiol Rev. 1991 Oct;71(4):1081–1115. doi: 10.1152/physrev.1991.71.4.1081. [DOI] [PubMed] [Google Scholar]
- Gombos Z., Vigh L. Primary Role of the Cytoplasmic Membrane in Thermal Acclimation Evidenced in Nitrate-Starved Cells of the Blue-Green Alga, Anacystis nidulans. Plant Physiol. 1986 Feb;80(2):415–419. doi: 10.1104/pp.80.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gombos Z., Wada H., Murata N. The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8787–8791. doi: 10.1073/pnas.91.19.8787. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gombos Z., Wada H., Murata N. 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. 1992 Oct 15;89(20):9959–9963. doi: 10.1073/pnas.89.20.9959. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Incharoensakdi A., Takabe T., Akazawa T. Effect of Betaine on Enzyme Activity and Subunit Interaction of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase from Aphanothece halophytica. Plant Physiol. 1986 Aug;81(4):1044–1049. doi: 10.1104/pp.81.4.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kanervo E., Aro E. M., Murata N. Low unsaturation level of thylakoid membrane lipids limits turnover of the D1 protein of photosystem II at high irradiance. FEBS Lett. 1995 May 8;364(2):239–242. doi: 10.1016/0014-5793(95)00404-w. [DOI] [PubMed] [Google Scholar]
- Ko R., Smith L. T., Smith G. M. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol. 1994 Jan;176(2):426–431. doi: 10.1128/jb.176.2.426-431.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lever M., Sizeland P. C., Bason L. M., Hayman C. M., Chambers S. T. Glycine betaine and proline betaine in human blood and urine. Biochim Biophys Acta. 1994 Aug 18;1200(3):259–264. doi: 10.1016/0304-4165(94)90165-1. [DOI] [PubMed] [Google Scholar]
- Murata N. Low-temperature effects on cyanobacterial membranes. J Bioenerg Biomembr. 1989 Feb;21(1):61–75. doi: 10.1007/BF00762212. [DOI] [PubMed] [Google Scholar]
- Murata N., Mohanty P. S., Hayashi H., Papageorgiou G. C. Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett. 1992 Jan 20;296(2):187–189. doi: 10.1016/0014-5793(92)80376-r. [DOI] [PubMed] [Google Scholar]
- Nomura M., Ishitani M., Takabe T., Rai A. K., Takabe T. Synechococcus sp. PCC7942 Transformed with Escherichia coli bet Genes Produces Glycine Betaine from Choline and Acquires Resistance to Salt Stress. Plant Physiol. 1995 Mar;107(3):703–708. doi: 10.1104/pp.107.3.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ono T. A., Murata N. Chilling Susceptibility of the Blue-green Alga Anacystis nidulans: I. EFFECT OF GROWTH TEMPERATURE. Plant Physiol. 1981 Jan;67(1):176–181. doi: 10.1104/pp.67.1.176. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rudolph A. S., Crowe J. H., Crowe L. M. Effects of three stabilizing agents--proline, betaine, and trehalose--on membrane phospholipids. Arch Biochem Biophys. 1986 Feb 15;245(1):134–143. doi: 10.1016/0003-9861(86)90197-9. [DOI] [PubMed] [Google Scholar]
- Rudolph A. S., Goins B. The effect of hydration stress solutes on the phase behavior of hydrated dipalmitoylphosphatidylcholine. Biochim Biophys Acta. 1991 Jul 1;1066(1):90–94. doi: 10.1016/0005-2736(91)90255-7. [DOI] [PubMed] [Google Scholar]
- Santoro M. M., Liu Y., Khan S. M., Hou L. X., Bolen D. W. Increased thermal stability of proteins in the presence of naturally occurring osmolytes. Biochemistry. 1992 Jun 16;31(23):5278–5283. doi: 10.1021/bi00138a006. [DOI] [PubMed] [Google Scholar]
- Stanier R. Y., Kunisawa R., Mandel M., Cohen-Bazire G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev. 1971 Jun;35(2):171–205. doi: 10.1128/br.35.2.171-205.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wada H., Gombos 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 May 10;91(10):4273–4277. doi: 10.1073/pnas.91.10.4273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wada H., Gombos Z., Murata N. Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature. 1990 Sep 13;347(6289):200–203. doi: 10.1038/347200a0. [DOI] [PubMed] [Google Scholar]
- Winzor C. L., Winzor D. J., Paleg L. G., Jones G. P., Naidu B. P. Rationalization of the effects of compatible solutes on protein stability in terms of thermodynamic nonideality. Arch Biochem Biophys. 1992 Jul;296(1):102–107. doi: 10.1016/0003-9861(92)90550-g. [DOI] [PubMed] [Google Scholar]
- Yamamoto H. Y., Bangham A. D. Carotenoid organization in membranes. Thermal transition and spectral properties of carotenoid-containing liposomes. Biochim Biophys Acta. 1978 Feb 2;507(1):119–127. doi: 10.1016/0005-2736(78)90379-6. [DOI] [PubMed] [Google Scholar]
- Yancey P. H., Clark M. E., Hand S. C., Bowlus R. D., Somero G. N. Living with water stress: evolution of osmolyte systems. Science. 1982 Sep 24;217(4566):1214–1222. doi: 10.1126/science.7112124. [DOI] [PubMed] [Google Scholar]