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Excretion of Ribitol and Sucrose by Green Algae Into the Culture Medium

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Excretion of Ribitol and Sucrose by Green Algae Into the Culture Medium [Agr. Biol. Chem., Vol. 29, No. 12, p. 1084•`1089, 1965] Excretion of Ribitol and Sucrose by Green Algae into the Culture Medium By Bunji MARUO,Toshie HATTORIand Hajime TAKAHASHI Instituteof AppliedMicrobiology, The Universityo f Tokyo,Tokyo ReceivedJune 18, 1965 Among 8 strains of algae grown with C14O2 as a sole source of carbon, two species of Trebouxia produced appreciable amounts of two photosynthetic products in the culture medium. One of them was identified as sucrose by cochromatography and by acid hydrolysis. The other compound was identified as ribitol by paper chromatography, paper electrophoresis, periodic acid oxidation, recrystallization with authentic ribitol and finally by the enzymatic method with ribitol dehydrogenase. Not so many organic compounds have been was obtained from the Division of Taxonomy of known to be excreted by green algae into the this Institute. culture medium. Thus, Tolbert1) showed that Culture conditions. Five ml of the salt medium, suitable for growth of each alga as described by Chlorella pyrenoidosa excreted a small amount Watanabe,3) were put into a test tube to which a of glycolic acid and Allen2) observed that filter paper section (1.5•~7cm, Toyo filter paper no. Chlamydomonas species accumulated glycolic 51, Toyo Roshi Co., Tokyo) was dipped in. The acid, oxalic acid and provably pyruvic acid. test tube with cotton plug was sterilized by autoclav The purpose of the present study has been ing, and was inoculated a roopful of alga onto the to re-examine, by the help of isotopic carbon, paper. After inoculation, 5 to 6 tubes were placed the accumulation of organic compounds by in a glass jar (5 liter) which contained 0.8 to 1% green algae in the culture medium. (v/v) of C14O2 (specific activity 0.5mc/mmole of Among 8 strains of algae cultured with carbon). The jar was illuminated by a 32 W circular C14O2 as a sole source of carbon, two species fluorescent lamp and the culture was continued for belonging to Trebouxia were found to produce 20 to 30 days at 20 to 25°C. Treatment of the culture. The incubation was large amounts of two photosynthetic products stopped by evacuating the remaining C14O2 from the in the medium. These compounds were glass jar. Cells from 5ml culture were collected by identified as sucrose and ribitol. This com centrifugation at 2,000•~g for 5min., and were munication describes the isolation and charac washed with 1ml of water. The combined super- terization of these two compounds. natant solutions were filled up to 20 ml by water and were called the "medium fraction" The washed MATERIALS AND METHODS cells were extracted with 1 ml of boiling 80% ethanoll Organisms. Following 8 strains of algae were for 30 min. and were washed once with 1 ml of 80% obtained from the Division of Biosynthesis II of ethanol. The combined ethanol solutions were filled this Institute: Trebouxia glomerate, Trebouxia erici, up to 20 ml by 80% ethanol and were called "ethanol Tolypothrix tenuis, Nostoc species, Calothrix brevissima, fraction" Phormidium angustissimum, Phormidium jadinianum and Paper chromatography and autoradiography. Chlorella elliposidea. Aerobacter aerogenes ATCC 9621 Two dimensional paper chromatography was carried 1) N. E. Tolbert and L. P. Zill, J. Biol. Chem., 222, 895 out with phenol-water and butanol-propionic acid- (1956). 2) M. B. Allen, Arch. Mikrobiol., 24, 163 (1956). 3) A. Watanabe, J. Gen. Appl. Microbiol., 6, 283 (1960). Excretion of Ribitol and Sucrose by Green Algae into the Culture Medium 1085 water systems according to the method of Benson and formaldehyde to the dimedone solution was carried his coworkers.4) Sugars were developed by aniline out overnight at room temperature. The needle hydrogen phthalate reagent. Autoradiogram was crystals appeared in the dimedone solution were taken with non-screen X-ray films (Fuji Photo. Film collected by centrifugation and were recrystallized Co., Ltd. Tokyo). from ethanol and water. The total radioactivity of Electrophoresis. The paper electrophoresis of formaldehyde formed was calculated by multiplying the specific activity of the dimedone complex by the polyalcohols was carried out with borate buffer con taining NaCl at pH 7.0, 8.0, and 9.2 at 1 mA(cm theoretical yield of the formaldehyde obtainable from according to the method of Consden et al.5) the carrier ribitol. The amounts of the radioactive Assay of radioactivity. Counting of paper chro compound was neglegible as compared to those of matograms were done with a conventional Geiger the carrier. Barium formate which remained in the counter (Irigaku Kenkyujo, Tokyo), after the spots alkali side arm was recrystallized twice from ethanol- were located by autoradiography. All other countings water, and the total radioactivity was calculated in were carried out by a liquid scintillation spectrometer the same manner as above. Ribitol dehydrogenase (Ec 1. 1. 1. c; ribitol:NAD (Tri-Carb model 314 AX, Packard Instrument Com oxidoreductase). The enzyme was extracted from pany, La Grange, Illinois) with hyamine-water- dioxane solvent system as reported previously.6) A. acre genes and purified according to the method of Fromm et al.s) The final purification step, calcium Correction for quenching was done by the ratio method.,) The corrected radioactivity was expressed phosphate gel treatment, however, was omitted. The as disintegration/min. (d./min.). purified preparation had the activity of 5.2 units/mg Periodate oxidation. An apparatus, used for the protein. The purified enzyme was specific for NAD and catalyzed the following reversible reaction: oxidation and equipped with two side arms, was essentially the same as described by Calvin and his Ribitol+NAD_??_D-Ribulose+NADH2 associates8) as a wet oxidation vessel. To the frozen sample (3.4ml aqueous solution containing 50ƒÊmoles The standard assay mixture contained 400ƒÊmoles of of carrier ribitol) in one side arm was added 0.5ml Tris-HCI, pH 7.5, 41ƒÊmoles of NAD, 4ƒÊmoles of ribitol and appropriate amount of enzyme in a total of 0.5N periodic acid. The whole apparatus was evacuated to 10-3mmHg with the aid of mechanical volume of 2.3 ml. The reaction was followed by a spectrophotometer (Type OR 50, Shimazu Co., Tokyo) and mercury diffusion pumps. After evacuation, the oxidation was carried out at room temperature for at 340mƒÊ at room temperature. When radioactive 2 hours with occasional shaking. After the oxidation, compound was oxidized by the enzyme, the reaction was stopped by boiling at 100°C for 10 min. The all volatile compounds in the mixture were distilled into the other side arm by heating the reaction side mixture was then treated with 100 mg of Norit in order to remove the nucleotides and the enzyme. arm finally to 60•Ž and by chilling the receiving side arm in liquid nitrogen. The remaining fraction The clear supernatant was subjected to paper chro in the reaction side arm after distillation was called matography. "nonvolatile fraction" The distillate was frozen by Reagents. Ribitol used in this experiment was a dry ice-ethanol bath and 0.4 ml of OA N Ba(OH)2 either a gift of Dr. Matsui of this University or the commertial preparation obtained from Nutritional were added. The new side arm containing 10 ml of Biochemicals Corporation (Cleveland, Ohio). D- 0.4% dimedone was attached to the apparatus and Ribulose were prepared according to Schmidtis) from evacuated for a short time with a water aspirator while keeping the distillate and the alkali in frozen D-ribulose o-nitrophenyl hydrazone purchased from state. After evacuation, distillation of the resulting Calbiochem (Los Angeles, California). NAD was the product of Sigma Chemicals Corporation (St Louis, 4) A. A. Benson, J. A. Bassham, M. Calvin, T. C. Goodale, V.A. Haas and W. Stepka, J. Am. Chem. Soc., 72,1710 (1950). Missouri). All other chemicals were commercial 5) R. Consden and W. M_ Stanier, Nature, 169, 783 (1952). preparations of reagent grade. 6) H. Takahashi, T. Hattori and B. Maruo. Anal. Chem., 35, 1982 (1963). 7) H. Takahashi, T. Hattori and B. Maruo, Anal. Biochem., 9) R. C. Nordlie and H. J. Fromm, in Hans-Ulrich Bergmyer, 2, 447 (1961). "Methods of Enzymatic Analysis" 8) M. Calvin, C. Heidelberger, J. C. Reid, B. M. Tolbert , Academic Press, New and P. E. Yankwich, "Isotopic Carbon". John Wiley and York, 1963, p. 184. 10) O. T. Schmidt and R. Treiber, Ber., 66, 1769 (1933). Sons, New York, 1949, p. 93. 1086 Bunji MARUO, Toshie HATTORI and Hajime TAKAHASHI RESULTS TABLE I. DISTRIBUTION OF RADIOACTIVITY AMONG Among 8 species of algae tested, Trebouxia THE PHOTOSYNTHETIC PRODUCTS erici and T. glomerata produced large amounts of photosynthetic products in the medium fractions. Fig. 1 shows the autoradiogram of the paper chromatogram of this fraction of T erici. The compound having lower RF values (spot 1) and that having higher RF values (spot 2) were the main products by T erici. T. glomerata also produced these two com- pounds as judged by paper chromatography. The fractions, each 0.2 ml, were subjected to paper Appreciable radioactivities were found in the chromatography. The radioactive spots were counted by the Geiger counter. The distribution of radioactivity was origins of the paper in both cases. expressed as the percentage of each spot to the total The distribution of radioactivities among radioactivity. the assimilated C14 in the medium and ethanol in T. erici, thus the following treatments were fractions of the two species of Trebouxia was done with the medium fraction of this summarized in Table I. As can be seen, organism. approximately 25 to 40% of radioactivities Two compounds, spots 1, 2, were eluted were found in spot 1 compound and 20 to from the paper chromatogram with water and 25% were in spot 2 compound in both medium were subjected to chemical analyses.
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