Subcellular distribution of central carbohydrate metabolism pathways in the red alga Cyanidioschyzon merolae
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Comprehensive subcellular localization analysis revealed that the subcellular distribution of carbohydrate metabolic pathways in the red alga Cyanidioschyzon is essentially identical with that in Arabidopsis , except the lack of transaldolase.
In plants, the glycolysis and oxidative pentose phosphate pathways (oxPPP) are located in both cytosol and plastids. However, in algae, particularly red algae, the subcellular localization of enzymes involved in carbon metabolism is unclear. Here, we identified and examined the localization of enzymes related to glycolysis, oxPPP, and tricarboxylic acid (TCA) and Calvin–Benson cycles in the red alga Cyanidioschyzon merolae. A gene encoding transaldolase of the oxPPP was not found in the C. merolae genome, and no transaldolase activity was detected in cellular extracts. The subcellular localization of 65 carbon metabolic enzymes tagged with green fluorescent protein or hemagglutinin was examined in C. merolae cells. As expected, TCA and Calvin–Benson cycle enzymes were localized to mitochondria and plastids, respectively. The analyses also revealed that the cytosol contains the entire glycolytic pathway and partial oxPPP, whereas the plastid contains a partial glycolytic pathway and complete oxPPP, with the exception of transaldolase. Together, these results suggest that the subcellular distribution of carbohydrate metabolic pathways in C. merolae is essentially identical with that reported in the photosynthetic tissue of Arabidopsis thaliana; however, it appears that substrates typically utilized by transaldolase are consumed by glycolytic enzymes in the plastidic oxPPP of C. merolae.
KeywordsGlycolysis Oxidative pentose phosphate pathway Tricarboxylic acid cycle Calvin–Benson cycle Subcellular localization Red algae
The authors thank Dr. H. Yoshikawa and Dr. S. Watanabe of the Tokyo University of Agriculture for providing pCG1 plasmid, and also thank Dr. M. Ohnuma and T. Kuroiwa of Rikkyo University for providing plasmid pBSHAb-T3′. This work was supported in part by Core Research for Evolutional Science and Technology (CREST) from the Japan Science and Technology Agency (JST), and Grants-in-Aid for Young Scientists (B) from JSPS (No. 25870155).
- Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C, Garavito RM, Benning C, Weber AP (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 differences in carbohydrate metabolism of both algae. Plant Physiol 137:460–474PubMedCentralPubMedCrossRefGoogle Scholar
- Collén J, Porcel B, Carré W, Ball SG, Chaparro C, Tonon T, Barbeyron T, Michel G, Noel B, Valentin K, Elias M, Artiguenave F, Arun A, Aury JM, Barbosa-Neto JF, Bothwell JH, Bouget FY, Brillet L, Cabello-Hurtado F, Capella-Gutiérrez S, Charrier B, Cladière L, Cock JM, Coelho SM, Colleoni C, Czjzek M, Da Silva C, Delage L, Denoeud F, Deschamps P, Dittami SM, Gabaldón T, Gachon CM, Groisillier A, Hervé C, Jabbari K, Katinka M, Kloareg B, Kowalczyk N, Labadie K, Leblanc C, Lopez PJ, McLachlan DH, Meslet-Cladiere L, Moustafa A, Nehr Z, Nyvall Collén P, Panaud O, Partensky F, Poulain J, Rensing SA, Rousvoal S, Samson G, Symeonidi A, Weissenbach J, Zambounis A, Wincker P, Boyen C (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci 110:5247–5252PubMedCentralPubMedCrossRefGoogle Scholar
- Dennis DT, Miernyk JA (1982) Compartmentation of nonphotosynthetic carbohydrate metabolism. Annu Rev Plant Physiol 33:27–50Google Scholar
- Imoto Y, Kuroiwa H, Yoshida Y, Ohnuma M, Fujiwara T, Yoshida M, Nishida K, Yagisawa F, Hirooka S, Miyagishima SY, Misumi O, Kawano S, Kuroiwa T (2013) Single-membrane-bounded peroxisome division revealed by isolation of dynamin-based machinery. Proc Natl Acad Sci 110:9583–9588PubMedCentralPubMedCrossRefGoogle Scholar
- Kroth PG, Chiovitti A, Gruber A, Martin-Jezequel V, Mock T, Parker MS, Stanley MS, Kaplan A, Caron L, Weber T, Maheswari U, Armbrust EV, Bowler C (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3:e1426PubMedCentralPubMedCrossRefGoogle Scholar
- Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657PubMedCrossRefGoogle Scholar
- Muñoz-Bertomeu J, Cascales-Miñana B, Mulet JM, Baroja-Fernández E, Pozueta-Romero J, Kuhn JM, Segura J, Ros R (2009) Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. Plant Physiol 151:541–558PubMedCentralPubMedCrossRefGoogle Scholar
- Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, Nakayama I, Ito F, Nakajima K, Sano M, Wada T, Kuhara S, Inouye K, Gojobori T, Ikeo K (2013) The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One 8:e57122PubMedCentralPubMedCrossRefGoogle Scholar
- Nishida K, Misumi O, Yagisawa F, Kuroiwa H, Nagata T, Kuroiwa T (2004) Triple immunofluorescent labeling of FtsZ, dynamin, and EF-Tu reveals a loose association between the inner and outer membrane mitochondrial division machinery in the red alga Cyanidioschyzon merolae. J Histochem Cytochem 52:843–849PubMedCrossRefGoogle Scholar
- Nozaki H, Takano H, Misumi O, Terasawa K, Matsuzaki M, Maruyama S, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Takio S, Tamura K, Chung SJ, Nakamura S, Kuroiwa H, Tanaka K, Sato N, Kuroiwa T (2007) A 100 %-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28PubMedCentralPubMedCrossRefGoogle Scholar
- Plancke C, Vigeolas H, Höhner R, Roberty S, Emonds-Alt B, Larosa V, Willamme R, Duby F, Onga Dhali D, Thonart P, Hiligsmann S, Franck F, Eppe G, Cardol P, Hippler M, Remacle C (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 77:404–417PubMedCrossRefGoogle 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 6:1006–1017PubMedCentralPubMedCrossRefGoogle Scholar
- Schönknecht G, Chen W, Ternes CM, Barbier GG, Shrestha RP, Stanke M, Bräutigam A, Baker BJ, Banfield JF, Garavito RM, Carr K, Wilkerson C, Rensing SA, Gagneul D, Dickenson NE, Oesterhelt C, Lercher MJ, Weber AP (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210PubMedCrossRefGoogle Scholar