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Carbon Metabolism

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Cyanidioschyzon merolae

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Abstract

Photosynthetic eukaryotes synthesize organic compounds through photosynthesis. The compounds are then consumed for energy production or converted into other compounds through various metabolic pathways in organelles. Recently, studies on carbohydrate and lipid metabolism were performed on the red alga Cyanidioschyzon merolae. These studies were possible due to advancements in genomics and transformation techniques. The C. merolae genome encodes enzymes related to basic carbohydrate and lipid metabolism, and the subcellular distribution of metabolic pathways of C. merolae is basically identical to that of land plants. However, some metabolic enzymes, such as NAD-dependent malic enzyme, glyoxylate cycle enzymes, some mitochondrial translocators, and several fatty acid desaturases, are not found in C. merolae, indicating the metabolic pathways of C. merolae are simpler than those of green plants. In this chapter, we will summarize our current understanding of carbon metabolism and describe unique features of C. merolae metabolism by comparing metabolic enzymes among different species of sequenced red algae.

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References

  • Araki S, Sakurai T, Omata T et al (1986) Lipid and fatty acid composition in the red alga Porphyra yezoensis. Jpn J Phycol 34:94–100

    CAS  Google Scholar 

  • Araki S, Sakurai T, Kawaguchi A, Murata N (1987) Positional distribution of fatty acids in glycerolipids of the marine red alga, Porphyra yezoensis. Plant Cell Physiol 28:761–766

    Article  CAS  Google Scholar 

  • Araki S, Sakurai T, Oohusa T et al (1989) Characterization of sulfoquinovosyl diacylglycerol from marine red algae. Plant Cell Physiol 30:775–781

    CAS  Google Scholar 

  • Awai K, Ohta H, Sato N (2014) Oxygenic photosynthesis without galactolipids. Proc Natl Acad Sci U S A 111:13571–13575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbier G, Oesterhelt C, Larson MD et al (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant. Plant Physiol 137:460–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharya D, Price DC, Chan CX et al (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941

    Article  PubMed  PubMed Central  Google Scholar 

  • Bricker DK, Taylor EB, Schell JC et al (2012) A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 337:96–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burgess SJ, Taha H, Yeoman JA et al (2016) Identification of the elusive pyruvate reductase of Chlamydomonas reinhardtii chloroplasts. Plant Cell Physiol 57:82–94

    Article  CAS  PubMed  Google Scholar 

  • Catt JW, Hills GJ, Roberts K (1978) Cell wall glycoproteins from Chlamydomonas reinhardii, and their self-assembly. Planta 138:91–98

    Article  CAS  PubMed  Google Scholar 

  • Cole LK, Vance JE, Vance DE (2012) Phosphatidylcholine biosynthesis and lipoprotein metabolism. Biochim Biophys Acta 1821:754–761

    Article  CAS  PubMed  Google Scholar 

  • Collén J, Porcel B, Carré W et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A 110:5247–5252

    Article  PubMed  PubMed Central  Google Scholar 

  • De Luca P, Moretti A (1983) Floridosides in Cyanidium caldarium, Cyanidioschyzon merolae and Galdieria sulphuraria (Rhodophyta, Cyanidiophyceae). J Phycol 19:368–369

    Article  Google Scholar 

  • Dennis D, Miernyk J (1982) Compartmentation of nonphotosynthetic carbohydrate metabolism. Annu Rev Plant Physiol 33:27–50

    Article  CAS  Google Scholar 

  • Deschamps P, Colleoni C, Nakamura Y et al (2008) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Ajjawi I, Manoli A et al (2009) Fatty acid desaturase4 of Arabidopsis encodes a protein distinct from characterized fatty acid desaturases. Plant J 60:832–839

    Article  CAS  PubMed  Google Scholar 

  • Gibellini F, Smith TK (2010) The Kennedy pathway-De novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 62:414–428

    Article  CAS  PubMed  Google Scholar 

  • Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59:115–142

    Article  CAS  PubMed  Google Scholar 

  • Gretz MR, Aronson JM, Sommerfeld MR (1980) Cellulose in the cell walls of the bangiophyceae (rhodophyta). Science 207:779–781

    Article  CAS  PubMed  Google Scholar 

  • Gross W, Schnarrenberger C (1995) Heterotrophic growth of two strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol 36:633–638

    CAS  Google Scholar 

  • Gruber A, Weber T, Bártulos CR et al (2009) Intracellular distribution of the reductive and oxidative pentose phosphate pathways in two diatoms. J Basic Microbiol 49:58–72

    Article  CAS  PubMed  Google Scholar 

  • Herzig S, Raemy E, Montessuit S et al (2012) Identification and functional expression of the mitochondrial pyruvate carrier. Science 337:93–96

    Article  CAS  PubMed  Google Scholar 

  • Hirabaru C, Izumo A, Fujiwara S et al (2010) The primitive rhodophyte Cyanidioschyzon merolae contains a semiamylopectin-type, but not an amylose-type, α-glucan. Plant Cell Physiol 51:682–693

    Article  CAS  PubMed  Google Scholar 

  • Imamura S, Kawase Y, Kobayashi I et al (2015) Target of rapamycin (TOR) plays a critical role in triacylglycerol accumulation in microalgae. Plant Mol Biol 89:309–318

    Article  CAS  PubMed  Google Scholar 

  • Jenner HL, Winning BM, Millar AH et al (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol 126:1139–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot Cell 12:776–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joyard J, Ferro M, Masselon C et al (2010) Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Prog Lipid Res 49:128–158

    Article  CAS  PubMed  Google Scholar 

  • Katayama K, Sakurai I, Wada H (2004) Identification of an Arabidopsis thaliana gene for cardiolipin synthase located in mitochondria. FEBS Lett 577:193–198

    Article  CAS  PubMed  Google Scholar 

  • Khozin-Goldberg I, HZ Y, Adlerstein D et al (2000) Triacylglycerols of the red microalga Porphyridium cruentum can contribute to the biosynthesis of eukaryotic galactolipids. Lipids 35:881–889

    Article  CAS  PubMed  Google Scholar 

  • Li C-L, Wang M, Ma X-Y, Zhang W (2014) NRGA1, a putative mitochondrial pyruvate carrier, mediates ABA regulation of guard cell ion channels and drought stress responses in Arabidopsis. Mol Plant 7:1508–1521

    Article  CAS  PubMed  Google Scholar 

  • Li-Beisson Y, Shorrosh B, Beisson F et al (2013) Acyl-lipid metabolism. Arab B 11:e0161

    Article  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-I T et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

  • Melo T, Alves E, Azevedo V et al (2015) Lipidomics as a new approach for the bioprospecting of marine macroalgae – unraveling the polar lipid and fatty acid composition of Chondrus crispus. Algal Res 8:181–191

    Article  Google Scholar 

  • Merchant SS, Kropat J, Liu B et al (2012) TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23:352–363

    Article  CAS  PubMed  Google Scholar 

  • Misumi O, Matsuzaki M, Nozaki H et al (2005) Cyanidioschyzon merolae genome. A tool for facilitating comparable studies on organelle biogenesis in photosynthetic eukaryotes. Plant Physiol 137:567–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mongrand S, Bessoule J-J, Cabantous F, Cassagne C (1998) The C16:3/C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry 49:1049–1064

    Article  CAS  Google Scholar 

  • Mori N, Moriyama T, Toyoshima M, Sato N (2016) Construction of global acyl lipid metabolic map by comparative genomics and subcellular localization analysis in the red alga Cyanidioschyzon merolae. Front Plant Sci 7:958

    PubMed  PubMed Central  Google Scholar 

  • Moriyama T, Sakurai K, Sekine K, Sato N (2014) Subcellular distribution of central carbohydrate metabolism pathways in the red alga Cyanidioschyzon merolae. Planta 240:585–598

    Article  CAS  PubMed  Google Scholar 

  • Moriyama T, Mori N, Sato N (2015) Activation of oxidative carbon metabolism by nutritional enrichment by photosynthesis and exogenous organic compounds in the red alga Cyanidioschyzon merolae: evidence for heterotrophic growth. Springer Plus 4:559

    Google Scholar 

  • Mukai LS, Craigie JS, Brown RG (1981) Chemical composition and structure of the cell walls of the Conchocelis and thallus phases of Porphyra tenera (Rhodophyceae). J Phycol 17:192–198

    Article  CAS  Google Scholar 

  • Nakahigashi K, Toya Y, Ishii N et al (2009) Systematic phenome analysis of Escherichia coli multiple-knockout mutants reveals hidden reactions in central carbon metabolism. Mol Syst Biol 5:306

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakamura Y, Sasaki N, Kobayashi M et al (2013) The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One 8:e57122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naumann I, Darsow KH, Walter C et al (2007) Identification of sulfoglycolipids from the alga Porphyridium purpureum by matrix-assisted laser desorption/ionisation quadrupole ion trap time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 21:3185–3192

    Article  CAS  PubMed  Google Scholar 

  • Nichols B, Appleby R (1969) The distribution and biosynthesis of arachidonic acid in algae. Phytochemistry 8:1907–1915

    Article  CAS  Google Scholar 

  • Nozaki H, Takano H, Misumi O et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28

    Article  PubMed  PubMed Central  Google Scholar 

  • Oh SH, Han JG, Kim Y et al (2009) Lipid production in Porphyridium cruentum grown under different culture conditions. J Biosci Bioeng 108:429–434

    Article  CAS  PubMed  Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pade N, Linka N, Ruth W et al (2015) Floridoside and isofloridoside are synthesized by trehalose 6-phosphate synthase-like enzymes in the red alga Galdieria sulphuraria. New Phytol 205:1227–1238

    Article  CAS  PubMed  Google Scholar 

  • Pettitt T, Jones A, Harwood J (1989) Lipids of the marine red algae, Chondrus crispus and Polysiphonia lanosa. Phytochemistry 28:399–405

    Article  CAS  Google Scholar 

  • Plancke C, Colleoni C, Deschamps P et al (2008) Pathway of cytosolic starch synthesis in the model glaucophyte Cyanophora paradoxa. Eukaryot Cell 7:247–257

    Article  CAS  PubMed  Google Scholar 

  • Plancke C, Vigeolas H, Höhner R et al (2014) Lack of isocitrate lyase in Chlamydomonas leads to changes in carbon metabolism and in the response to oxidative stress under mixotrophic growth. Plant J 77:404–417

    Article  CAS  PubMed  Google Scholar 

  • Popper ZA, Michel G, Hervé C et al (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590

    Article  CAS  PubMed  Google Scholar 

  • Pracharoenwattana I, Cornah JE, Smith SM (2005) Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination. Plant Cell 17:2037–2048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raven J, Johnston A, MacFarlane J (1990) Carbon metabolism. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Roberts E, Roberts AW (2009) A cellulose synthase (CESA) gene from the red alga Porphyra yezoensis (Rhodophyta). J Phycol 45:203–212

    Article  CAS  PubMed  Google Scholar 

  • Sakurai T, Aoki M, Ju X et al (2016) Profiling of lipid and glycogen accumulations under different growth conditions in the sulfothermophilic red alga Galdieria sulphuraria. Bioresour Technol 200:861–866

    Article  CAS  PubMed  Google Scholar 

  • Sato N, Moriyama T (2007) Genomic and biochemical analysis of lipid biosynthesis in the unicellular rhodophyte Cyanidioschyzon merolae: lack of a plastidic desaturation pathway results in the coupled pathway of galactolipid synthesis. Eukaryot Cell 6:1006–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato N, Kobayashi S, Aoki M et al (2016a) Identification of genes for sulfolipid synthesis in primitive red alga Cyanidioschyzon merolae. Biochem Biophys Res Commun 470:123–129

    Article  CAS  PubMed  Google Scholar 

  • Sato N, Mori N, Hirashima T, Moriyama T (2016b) Diverse pathways of phosphatidylcholine biosynthesis in algae as estimated by labeling studies and genomic sequence analysis. Plant J 87:281–292

    Article  CAS  PubMed  Google Scholar 

  • Sato N, Moriyama T, Mori N, Toyoshima M (2017) Lipid metabolism and potentials of biofuel and high added-value oil production in red algae. World J Microbiol Biotechnol 33:74

    Article  PubMed  Google Scholar 

  • Schönknecht G, Chen W-H, Ternes CM et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210

    Article  PubMed  Google Scholar 

  • Shimonaga T, Fujiwara S, Kaneko M et al (2007) Variation in storage alpha-polyglucans of red algae: amylose and semi-amylopectin types in Porphyridium and glycogen type in Cyanidium. Mar Biotechnol (NY) 9:192–202

    Article  CAS  Google Scholar 

  • Shimonaga T, Konishi M, Oyama Y et al (2008) Variation in storage alpha-glucans of the Porphyridiales (Rhodophyta). Plant Cell Physiol 49:103–116

    Article  CAS  PubMed  Google Scholar 

  • Siddhanta AK, Kumar S, Mehta GK et al (2013) Cellulose contents of some abundant Indian seaweed species. Nat Prod Commun 8:497–500

    CAS  PubMed  Google Scholar 

  • Sumiya N, Kawase Y, Hayakawa J et al (2015) Expression of cyanobacterial acyl-ACP reductase elevates the triacylglycerol level in the red alga Cyanidioschyzon merolae. Plant Cell Physiol 56:1962–1980

    Article  CAS  PubMed  Google Scholar 

  • Takusagawa M, Nakajima Y, Saito T, Misumi O (2016) Primitive red alga Cyanidioschyzon merolae accumulates storage glucan and triacylglycerol under nitrogen depletion. J Gen Appl Microbiol 62:111–117

    Article  CAS  PubMed  Google Scholar 

  • Toyoshima M, Mori N, Moriyama T et al (2016) Analysis of triacylglycerol accumulation under nitrogen deprivation in the red alga Cyanidioschyzon merolae. Microbiology 162:803–812

    Article  CAS  PubMed  Google Scholar 

  • Tronconi MA, Fahnenstich H, Gerrard Weehler MC et al (2008) Arabidopsis NAD-malic enzyme functions as a homodimer and heterodimer and has a major impact on nocturnal metabolism. Plant Physiol 146:1540–1552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyra HM, Linka M, Weber APM, Bhattacharya D (2007) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8:R212

    Article  PubMed  PubMed Central  Google Scholar 

  • Viola R, Nyvall P, Pedersén M (2001) The unique features of starch metabolism in red algae. Proc Biol Sci 268:1417–1422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vítová M, Goecke F, Sigler K, Řezanka T (2016) Lipidomic analysis of the extremophilic red alga Galdieria sulphuraria in response to changes in pH. Algal Res 13:218–226

    Article  Google Scholar 

  • Wada H, Shintani D, Ohlrogge J (1997) Why do mitochondria synthesize fatty acids? Evidence for involvement in lipoic acid production. Proc Natl Acad Sci U S A 94:1591–1596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber APM, Oesterhelt C, Gross W et al (2004) EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55:17–32

    Google Scholar 

  • Wiese A, Gröner F, Sonnewald U et al (1999) Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett 461:13–18

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Catalanotti C, D’Adamo S et al (2014) Alternative acetate production pathways in Chlamydomonas reinhardtii during dark anoxia and the dominant role of chloroplasts in fermentative acetate production. Plant Cell 26:4499–4518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Meguro-ku, Tokyo, Japan

    Takashi Moriyama, Natsumi Mori & Naoki Sato

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  1. Takashi Moriyama
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  2. Natsumi Mori
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  3. Naoki Sato
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Correspondence to Naoki Sato .

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Editors and Affiliations

  1. Faculty of Science Department of Chemical and Biological Sciences, Japan Women’s University, Tokyo, Japan

    Tsuneyoshi Kuroiwa

  2. Department of Cell Genetics, National Institute of Genetics, Shizuoka, Japan

    Shinya Miyagishima

  3. Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Chiba, Japan

    Sachihiro Matsunaga

  4. Department of Life Sciences Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan

    Naoki Sato

  5. Department of Biological Sciences Graduate School of Science, University of Tokyo, Tokyo, Japan

    Hisayoshi Nozaki

  6. Laboratory for Chemistry and Life Science Institute of Innovative Research, Tokyo Institute of Technology, Kanagawa, Japan

    Kan Tanaka

  7. Graduate School of Science and Technology for Innovation Faculty of Science, Department of Biological Science and Chemistry, Yamaguchi University, Yamaguchi, Japan

    Osami Misumi

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Moriyama, T., Mori, N., Sato, N. (2017). Carbon Metabolism. In: Kuroiwa, T., et al. Cyanidioschyzon merolae. Springer, Singapore. https://doi.org/10.1007/978-981-10-6101-1_19

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