Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-19T03:46:55.268Z Has data issue: false hasContentIssue false
  • English
  • Français

Composition and regulation of thylakoid membrane of Antarctic ice microalgae Chlamydomonas sp. ICE-L in response to low-temperature environment stress

Published online by Cambridge University Press:  06 May 2016

Wang Yi-Bin ,
Liu Fang-Ming ,
Zhang Xiu-Fang ,
Zhang Ai-Jun ,
Wang Bin ,
Zheng Zhou ,
Sun Cheng-Jun  and
Miao Jin-Lai
Wang Yi-Bin*
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Key Laboratory of Marine Bioactive Substances, SOA, Qingdao 266061, China
Liu Fang-Ming
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Key Laboratory of Marine Bioactive Substances, SOA, Qingdao 266061, China
Zhang Xiu-Fang
Affiliation:
Qingdao Hiser Hospital, Qingdao 266033, China
Zhang Ai-Jun
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Key Laboratory of Marine Bioactive Substances, SOA, Qingdao 266061, China
Wang Bin
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Key Laboratory of Marine Bioactive Substances, SOA, Qingdao 266061, China
Zheng Zhou
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Key Laboratory of Marine Bioactive Substances, SOA, Qingdao 266061, China
Sun Cheng-Jun
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
Miao Jin-Lai*
Affiliation:
First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Key Laboratory of Marine Bioactive Substances, SOA, Qingdao 266061, China
*
Correspondence should be addressed to:M. Jin-lai and W. Yi-bin, First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China email: miaojinlai@fio.org.cn; wangyibin@fio.org.cn
Correspondence should be addressed to:M. Jin-lai and W. Yi-bin, First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China email: miaojinlai@fio.org.cn; wangyibin@fio.org.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Ice algae have successfully adapted to the extreme environmental conditions in the Antarctic, however the underlying mechanisms involved in the regulation and response of thylakoid membranes and chloroplast to low-temperature stress are still not well understood. In this study, changes in pigment concentrations, lipids, fatty acids and pigment protein complexes in thylakoid membranes and chloroplast after exposure to low temperature conditions were investigated using the Antarctic ice algae Chlamydomonas sp. ICE-L. Results showed that the chloroplasts of Chlamydomonas sp. ICE-L are distributed throughout the cell except in the nuclear region in the form of thylakoid lamellas which exists in the gap between organelles and the starch granules. Also, the structure of mitochondria has no obvious change after cold stress. Concentrations of Chl a, Chl b, monogalactosyl diacylglycerol, digalactosyl diacylglycerol and fatty acids were also observed to exhibit changes with temperature, suggesting possible adaptations to cold environments. The light harvesting complex, lutein and β-carotene played an important role for adaptation of ICE-L, and increasing of monogalactosyl diacylglycerol and digalactosyl diacylglycerol improved the overall degree of unsaturation of thylakoid membranes, thereby maintaining liquidity of thylakoid membranes. The pigments, lipids, fatty acids and pigment-protein complexes maintained the stability of the thylakoid membranes and the normal physiological function of Chlamydomonas sp. ICE-L.

Keywords

Antarctic ice microalgaeChlamydomonas sp.chloroplastthylakoid membranecold stress response
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 6 , September 2017 , pp. 1241 - 1249
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allen, J.F. and Forsberg, J. (2001) Molecular recognition in thylakoid structure and function. Trends in Plant Science 6, 317–326.Google Scholar
Aronsson, H., Schöttler, M.A., Kelly, A.A., Sundqvist, C., Dörmann, P., Karim, S. and Jarvis, P. (2008) Monogalactosyl diacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiology 148, 580–592.Google Scholar
Arrigo, K.R., Worthen, D.L., Lizotte, M.P., Dixon, P. and Dieckmann, G. (1997) Primary production in Antarctic sea ice. Science 276, 394–397.Google Scholar
Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.Google Scholar
Bunt, J.S. and Wood, E.J.F. (1963) Microbiology of Antarctic sea-ice: microalgae and Antarctic sea-ice. Nature 199, 1254–1255.Google Scholar
Chen, Z., He, C.L. and Hu, H.H. (2012) Temperature responses of growth, photosynthesis, fatty acid and nitrate reductase in Antarctic and temperate Stichococcus . Extremophiles 16, 127–133.Google Scholar
D'Amico, S., Collins, T., Marx, J.C., Feller, G. and Gerday, C. (2006) Psychrophilic microorganisms: challenges for life. EMBO Report 7, 385–389.Google Scholar
Dolhi, J.M., Maxwell, D.P. and Morgan-Kiss, R.M. (2013) Review: the Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis. Extremophiles 17, 711–722.Google Scholar
Eddie, B., Krembs, C. and Neuer, S. (2008) Characterization and growth response to temperature and salinity of psychrophilic, halotolerant Chlamydomonas sp. ARC isolated from Chukchi sea ice. Marine Ecology Progress Series 354, 107–117.Google Scholar
Gounaris, K., Barber, J. and Harwood, J.L. (1986) The thylakoid membranes of higher plant chloroplasts. Biochemical Journal 237, 313–326.Google Scholar
Gudynaite-Savitch, L., Gretes, M., Morgan-Kiss, R.M., Savitch, L.V., Simmonds, J., Kohalmi, S.E. and Huner, N.P.A. (2006) Cytochrome f from the Antarctic psychrophile, Chlamydomonas raudensis UWO 241: structure, sequence, and complementation in the mesophile, Chlamydomonas reinhardtii . Molecular Genetics and Genomics 275, 387–398.Google Scholar
Hetherington, S.E. and Smillie, R.M. (1984) Practical applications of chlorophyll fluorescence in ecophysiology, physiology and plant breeding. Advances in Photosynthesis Research 4, 447–450.CrossRefGoogle Scholar
Huner, N.P.A., Krol, M., Williams, J.P., Maissan, E., Low, P.S., Roberts, D. and Thompson, J.E. (1987) Low temperature development induces a specific decrease in trans-Δ3- hexadecenoic acid content which influences LHCII organization. Plant Physiology 84, 12–18.CrossRefGoogle Scholar
Jagannadham, M.V., Chattopadhyay, M.K., Subbalakshmi, C., Vairamani, M., Narayanan, K., Rao, M.C. and Shivaji, S. (2000) Carotenoids of an Antarctic psychrotolerant bacterium Sphingobacterium antarcticus and a mesophilic bacterium Sphingobacterium multivorum . Archives of Microbiology 173, 418–424.CrossRefGoogle Scholar
Jeffrey, S.W. and Humphrey, G.F. (1975) New spectrophotometric equations for determining chlorophyll a, b, c, and c2 in higher plants algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167, 191–194.CrossRefGoogle Scholar
Li, B.B., Guo, J.K., Zhou, Y., Zhang, Z.Z. and Zhang, L.X. (2003) Blue native gel electrophoresis analysis of chloroplast pigment protein complexes. Progress in Biochemistry and Biophysics 30, 639–643.Google Scholar
Li, X., Hu, H.Y. and Zhang, Y.P. (2011) Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature. Bioresource Technology 102, 3098–3102.Google ScholarPubMed
Liu, C., Huang, X., Wang, X., Zhang, X. and Li, G. (2006) Phylogenetic studies on two strains of Antarctic ice algae based on morphological and molecular characteristics. Phycologia 45, 190–198.Google Scholar
Lyon, B.R. and Mock, T. (2014) Polar microalgae: new approaches towards understanding adaptations to an extreme and changing environment. Biology 3, 56–80. doi: 10.3390/biology3010056 Google Scholar
Macpherson, A.N. and Hiller, R.G. (2003) Light-harvesting systems in chlorophyll c-containing algae. Light-harvesting antennas in photosynthesis. Dordrecht: Springer, pp. 323–352.Google Scholar
McMinn, A., Martin, A. and Ryan, K. (2010) Phytoplankton and sea ice algal biomass and physiology during the transition between winter and spring (McMurdo Sound, Antarctica). Polar Biology 33, 1547–1556.Google Scholar
Morgan-Kiss, R.M., Priscu, J.C., Pocock, T., Gudynaite-Savitch, L. and Huner, N.P.A. (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiology and Molecular Biology Reviews 70, 222–252.Google Scholar
Murata, N., Higashi, S.I. and Fujimura, Y. (1990) Glycerolipids in various preparations of photosystem II from spinach chloroplasts. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1019, 261–268.CrossRefGoogle Scholar
Nagashima, H., Matsumoto, G.I., Ohtani, S. and Momose, H. (1995) Temperature acclimation and the fatty acid composition of an Antarctic green alga Chlorella (16th Symposium on Polar Biology). Proceedings of the NIPR Symposium on Polar Biology 8, 194–199.Google Scholar
Peter, G.F., and Thornber, J.P. (1991) Electrophoretic procedures for fractionation of photosystem I and II pigment-proteins of higher plants and for determination of their subunit composition. Methods in Plant Biochemistry 5, 195–210.Google Scholar
Poerschmann, J., Spijkerman, E. and Langer, U. (2004) Fatty acid patterns in Chlamydomonas sp. as a marker for nutritional regimes and temperature under extremely acidic conditions. Microbial Ecology 48, 78–89.CrossRefGoogle Scholar
Priscu, J.C., Palmisano, A.C., Peiscu, L.R. and Sullivan, C.W. (1989) Temperature dependence of inorganic nitrogen uptake and assimilation in Antarctic sea-ice microalgae. Polar Biology 9, 443–446.Google Scholar
Provasoli, L. (1968) Media and prospects for the cultivation of marine algae. In Proceedings of the U.S.-Japan Conference 1968, 63–95.Google Scholar
Routaboul, J.M., Fischer, S.F. and Browse, J. (2000) Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiology 124, 1697–1705.Google Scholar
Rüdiger, W. (2002) Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynthesis Research 74, 187–193.Google Scholar
Staehelin, L.A. (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynthesis Research 76, 185–196.Google Scholar
Staehelin, L.A. and Arntzen, C.J. (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. Journal of Cell Biology 97, 1327–1337.Google Scholar
Takeshi, I., Deshmukh, D.S. and Pieringers, R.A. (1971) The association of the galactosyl diglycerides of brain with myelination. Journal of Biological Chemistry 246, 5688–5694.Google Scholar
Teoh, M.L., Chu, W.L., Marchant, H. and Phang, S.M. (2004) Influence of culture temperature on the growth, biochemical composition and fatty acid profiles of six Antarctic microalgae. Journal of Applied Phycology 16, 421–430.CrossRefGoogle Scholar
Teoh, M.L., Phang, S.M. and Chu, W.L. (2013) Response of Antarctic, temperate, and tropical microalgae to temperature stress. Journal of Applied Phycology 25, 285–297.CrossRefGoogle Scholar
Thomas, D.N. and Dieckmann, G.S. (2002) Antarctic sea ice – a habitat for extremophiles. Science 295, 641–644.CrossRefGoogle ScholarPubMed
Thompson, G.A. Jr (1996) Lipids and membrane function in green algae. Biochimica et Biophysica Acta (BBA) –Lipids and Lipid Metabolism 1302, 17–45.CrossRefGoogle ScholarPubMed
Vijayan, P. and Browse, J. (2002) Photoinhibition in mutants of Arabidopsis deficient in thylakoid unsaturation. Plant Physiology 129, 876–885.Google Scholar
White, D.C., Davis, W.M., Nickels, J.S., King, J.D. and Bobbie, R.J. (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40, 51–62.Google Scholar
Wollman, F.A., Minaib, L. and Nechushtai, R. (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1411, 21–85.Google Scholar
Xu, Y.N. and Siegenthaler, P.A. (1996) Phosphatidylglycerol molecular species of photosynthetic membranes analyzed by high-performance liquid chromatography: theoretical considerations. Lipids 31, 223–229.CrossRefGoogle ScholarPubMed