Glycerolipid synthesis in Chlorella kessleri 11h. I. Existence of a eukaryotic pathway.

The fatty acid distributions at the sn-1 and sn-2 positions in major chloroplast lipids of Chlorella kessleri 11h, monogalactosyl diacylglycerol (MGDG) and digalactosyl diacylglycerol (DGDG), were determined to show the coexistence of both C16 and C18 acids at the sn-2 position, i.e. of prokaryotic and eukaryotic types in these galactolipids. For investigation of the biosynthetic pathway for glycerolipids in C. kessleri 11h, cells were fed with [14C]acetate for 30 min, and then the distribution of the radioactivity among glycerolipids and their constituent fatty acids during the subsequent chase period was determined. MGDG and DGDG were labeled predominantly as the sn-1-C18-sn-2-C16 (C18/C16) species as early as by the start of the chase, which suggested the synthesis of these lipids within chloroplasts via a prokaryotic pathway. On the other hand, the sn-1-C18-sn-2-C18 (C18/C18) species of these galactolipids gradually gained radioactivity at later times, concomitant with a decrease in the radioactivity of the C18/C18 species of phosphatidylcholine (PC). The change at later times can be explained by the conversion of the C18/C18 species of PC into galactolipids through a eukaryotic pathway. The results showed that C. kessleri 11h, distinct from most of other green algal species that were postulated mainly to use a prokaryotic pathway for the synthesis of chloroplast lipids, is similar to a group of higher plants designated as 16:3 plants in terms of the cooperation of prokaryotic and eukaryotic pathways to synthesize chloroplast lipids. We propose that the physiological function of the eukaryotic pathway in C. kessleri 11h is to supply chloroplast membranes with 18:3/18:3-MGDG for their functioning, and that the acquisition of a eukaryotic pathway by green algae was favorable for evolution into land plants.

[1]  N. Sato,et al.  Cloning of a gene for chloroplast omega6 desaturase of a green alga, Chlamydomonas reinhardtii. , 1997, Journal of biochemistry.

[2]  C. Bigogno,et al.  Elucidation of the Biosynthesis of Eicosapentaenoic Acid (EPA) in the Microalga Porphyridium Cruentum , 1997 .

[3]  C. Giroud,et al.  Lipids of Chlamydomonas reinhardtii. Analysis of Molecular Species and Intracellular Site(s) of Biosynthesis , 1988 .

[4]  G. A. Thompson,et al.  Lipids and membrane function in green algae. , 1996, Biochimica et biophysica acta.

[5]  Waldemar Eichenberger,et al.  Lipids of Pavlova lutheri: Cellular site and metabolic role of DGCC , 1997 .

[6]  J. Browse,et al.  Glycerolipid Synthesis: Biochemistry and Regulation , 1991 .

[7]  S. Miyachi,et al.  Quantum Requirements of Photosynthetic Oxygen Evolution and 77 K Fluorescence Emission Spectra in Unicellular Green Algae Grown Under Low‐ and High‐CO2‐Conditions , 1988 .

[8]  G. R. Jamieson,et al.  The component fatty acids of some marine algal lipids , 1972 .

[9]  S. Miyachi,et al.  EFFECTS OF CO2 CONCENTRATION DURING GROWTH ON THE INTRACELLULAR STRUCTURE OF CHLORELLA AND SCENEDESMUS (CHLOROPHYTA) 1 , 1986 .

[10]  S. Miyachi,et al.  The function of carbonic anhydrase in aquatic photosynthesis , 1989 .

[11]  G. A. Thompson,et al.  Quantitative analysis of Dunaliella salina diacylglyceryltrimethylhomoserine and its individual molecular species by high performance liquid chromatography , 1985 .

[12]  N. Murata,et al.  Positional Distribution of Fatty Acids in Glycerolipids of the Marine Red Alga, Porphyra yezoensis , 1987 .

[13]  B. Nichols Light induced changes in the lipids of Chlorella vulgaris. , 1965, Biochimica et biophysica acta.

[14]  Y. Nozawa,et al.  Molecular control of membrane properties during temperature acclimation. Fatty acid desaturase regulation of membrane fluidity in acclimating Tetrahymena cells. , 1976, Biochemistry.

[15]  W. J. Dyer,et al.  A rapid method of total lipid extraction and purification. , 1959, Canadian journal of biochemistry and physiology.

[16]  M. Frentzen,et al.  Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. , 2005, European journal of biochemistry.

[17]  N. Murata,et al.  Modes of Fatty-Acid Desaturation in Cyanobacteria , 1992 .

[18]  P. Roughan,et al.  CELLULAR ORGANIZATION OF GLYCEROLIPID METABOLISM , 1982 .

[19]  Murata Norio,et al.  Lipid biosynthesis in the blue-green alga, Anabaena variabilis: II. Fatty acids and lipid molecular species☆ , 1982 .

[20]  N. Sato,et al.  Effects of CO(2) Concentration during Growth on Fatty Acid Composition in Microalgae. , 1990, Plant physiology.

[21]  G. R. Jamieson,et al.  The fatty acid composition of Ulothrix aequalis lipids , 1976 .

[22]  S. Miyachi,et al.  Ultrastructure of Dunaliella tertiolecta Cells Grown under Low and High CO2 Concentrations , 1986 .

[23]  M. Mitz CO2 biodynamics: a new concept of cellular control. , 1979, Journal of theoretical biology.

[24]  M. Furuya,et al.  Isolation and Identification of Diacylglyceryl-O-4′-(N,N,N-trimethyl)-homoserine from the Fern Adiantum capillus-veneris L. , 1983 .

[25]  Murata Norio,et al.  Effect of growth temperature on lipid and fatty acid compositions in the blue-green algae, Anabaena variabilis and Anacystis nidulans. , 1979 .

[26]  A. Kaplan,et al.  CO2 CONCENTRATING MECHANISMS IN PHOTOSYNTHETIC MICROORGANISMS. , 1999, Annual review of plant physiology and plant molecular biology.

[27]  R. Safford,et al.  Positional distribution of fatty acids in monogalactosyl diglyceride fractions from leaves and algae. Structural and metabolic studies. , 1970, Biochimica et biophysica acta.

[28]  Z. Cohen,et al.  Elucidation of the Biosynthesis of Eicosapentaenoic Acid in the Microalga Porphyridium cruentum (II. Studies with Radiolabeled Precursors) , 1997, Plant physiology.

[29]  N. Sato,et al.  Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. , 1995, European journal of biochemistry.

[30]  A. T. James,et al.  Interrelationships between fatty acid biosynthesis and acyl-lipid synthesis in Chlorella vulgaris. , 1967, The Biochemical journal.

[31]  D. Stern,et al.  The Treasure Trove of Algal Chloroplast Genomes. Surprises in Architecture and Gene Content, and Their Functional Implications212 , 2002, Plant Physiology.

[32]  S. Miyachi,et al.  Effects of CO2 concentration during growth on subsequent photosynthetic CO2 fixation in Chlorella1 , 1977 .

[33]  N. Sato Lipids in Cryptomonas CR-1. II. Biosynthesis of Betaine Lipids and Galactolipids , 1991 .