Skip to main content

Advertisement

SpringerLink
Log in

EST-analysis of the thermo-acidophilic red microalga Galdieriasulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

When we think of extremophiles, organisms adapted to extreme environments, prokaryotes come to mind first. However, the unicellular red micro-alga Galdieria sulphuraria (Cyanidiales) is a eukaryote that can represent up to 90% of the biomass in extreme habitats such as hot sulfur springs with pH values of 0–4 and temperatures of up to 56 °C. This red alga thrives autotrophically as well as heterotrophically on more than 50 different carbon sources, including a number of rare sugars and sugar alcohols. This biochemical versatility suggests a large repertoire of metabolic enzymes, rivaled by few organisms and a potentially rich source of thermo-stable enzymes for biotechnology. The temperatures under which this organism carries out photosynthesis are at the high end of the range for this process, making G. sulphuraria a valuable model for physical studies on the photosynthetic apparatus. In addition, the gene sequences of this living fossil reveal much about the evolution of modern eukaryotes. Finally, the alga tolerates high concentrations of toxic metal ions such as cadmium, mercury, aluminum, and nickel, suggesting potential application in bioremediation. To begin to explore the unique biology of G. sulphuraria, 5270 expressed sequence tags from two different cDNA libraries have been sequenced and annotated. Particular emphasis has been placed on the reconstruction of metabolic pathways present in this organism. For example, we provide evidence for (i) a complete pathway for lipid A biosynthesis; (ii) export of triose-phosphates from rhodoplasts; (iii) and absence of eukaryotic hexokinases. Sequence data and additional information are available at http://genomics.msu.edu/galdieria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • AGI (The Arabidopsis Genome Initiative). 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Albertano, P., Ciniglia, C., Pinto, G. and Pollio, A. 2000. The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: An update. Hydrobiology 433: 137–143.

    Google Scholar 

  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.

    Google Scholar 

  • Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402.

    Google Scholar 

  • Bailey, R.W. and Staehelin, L.A. 1968. The chemical composition of isolated cell walls of Cyanidium caldarium. J. Gen. Microbiol. 54: 269–276.

    Google Scholar 

  • Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. and Wheeler, D.L. 2003. GenBank. Nucleic Acids Res. 31: 23–27.

    Google Scholar 

  • Benz, R. and Cros, D. 1978. Influence of sterols on ion transport through lipid bilayer membranes. Biochem. Biophys. Acta 506: 265–280.

    Google Scholar 

  • Benz, R., Cros, D., Janko, K., Lauger, P. and Stark, G. 1980. Effects of lipid structure on the kinetics of carrier-mediated ion transport. Acta Physiol. Scand. Suppl. 481: 47–52.

    Google Scholar 

  • Beudeker, R.F. and Tabita, F.R. 1983. Control of photorespiratory glycolate metabolism in an oxygen-resistant mutant of Chlorella sorokiniana. J. Bacteriol. 155: 650–656.

    Google Scholar 

  • Brock, T.D. 1973. Lower pH limit for the existence of bluegreen algae: Evolutionary and ecological implications. Science 179: 480–483.

    Google Scholar 

  • Brock, T.D.1978. The genus Cyanidium. In: T.D. Brock (Ed.), Thermophilic Microorganisms and Life at High Temperatures, Springer-Verlag, New York, pp. 255–302.

    Google Scholar 

  • Burdette, D.S., Jung, S.H., Shen, G.J., Hollingsworth, R.I. and Zeikus, J.G. 2002. Physiological function of alcohol dehydrogenases and long-chain (C(30)) fatty acids in alcohol tolerance of Thermoanaerobacter ethanolicus. Appl. Environ. Microbiol. 68: 1914–1918.

    Google Scholar 

  • Büttner, M. and Sauer, N. 2000. Monosaccharide transporters in plants: Structure, function and physiology. Biochim. Biophys. Acta 1465: 263–274.

    Google Scholar 

  • Cid, E., Geremia, R.A., Guinovart, J.J. and Ferrer, J.C. 2002. Glycogen synthase: towards a minimum catalytic unit? FEBS Lett. 528: 5–11.

    Google Scholar 

  • Cid, E., Gomis, R.R., Geremia, R.A., Guinovart, J.J. and Ferrer, J.C. 2000. Identification of two essential glutamic acid residues in glycogen synthase. J. Biol. Chem. 275: 33614–33621.

    Google Scholar 

  • Cozzolino, S., Caputo, P., De Castro, O., Moretti, A. and Pinto, G. 2000. Molecular variation in Galdieria sulphuraria (Galdieri) Merola and its bearing on taxonomy. Hydrobiology 433: 145–151.

    Google Scholar 

  • De Luca, P., Taddei, R. and Varano, L. 1978. Cyanidioschyzon merolae: A new alga of thermal acidic environments. Webbia 33: 37–44.

    Google Scholar 

  • Derelle, E., Ferraz, C., Lagoda, P., Eychenie, S., Cooke, R., Regad, F., Sabau, X., Courties, C., Delseny, M., Demaille, J., Picard, A. and Moreau, H. 2002. DNA libraries for sequencing the genome of Ostreococcus tauri (Chlorophyta, Prasinophyceae): The smallest free-living eukaryotic cell. J. Phycol. 38: 1150–1156.

    Google Scholar 

  • Doemel, W.N. and Brock, T.D. 1970. The upper temperature limit of Cyanidium caldarium. Arch Microbiol. 72: 326–332.

    Google Scholar 

  • Doemel, W.N. and Brock T.D. 1971. The physiolocial ecology of Cyanidium caldarium. J. Gen. Microbiol. 67: 17–32.

    Google Scholar 

  • Donachie, S.P., Christenson, B.W., Kunkel, D.D., Malahoff, A. and Alam, M. 2002. Microbial community in acidic hydrothermal waters of volcanically active White Island, New Zealand. Extremophiles 6: 419–425.

    Google Scholar 

  • Elferink, M.G.L., Dewit, J.G., Demel, R., Driessen, A.J.M. and Konings, W.N. 1992. Functional Reconstitution of Membrane Proteins in Monolayer Liposomes from Bipolar Lipids of Sulfolobus acidocaldarius. J. Biol. Chem. 267: 1375–1381.

    Google Scholar 

  • Ewing, B. and Green, P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186–194.

    Google Scholar 

  • Ewing, B. and Green, P. 2000. Analysis of expressed sequence tags indicates 35,000 human genes. Nat. Genet. 25: 232–234.

    Google Scholar 

  • Ewing, B., Hillier, L., Wendl, M.C. and Green, P. 1998. Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175–185.

    Google Scholar 

  • Flügge, U.I. 1999. Phosphate translocators in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 27–45.

    Google Scholar 

  • Flügge, U.I. and Weber, A. 1994. A rapid method for measuring organelle-specific substrate transport in homogenates from plant tissues. Planta 194: 181–185.

    Google Scholar 

  • Glöckner, G., Rosenthal, A. and Valentin, K. 2000. The structure and gene repertoire of an ancient red algal plastid genome. J. Mol. Evol. 51: 382–390.

    Google Scholar 

  • Goyal, A. 2002. Glycolate metabolism in algal chloroplasts: inhibition by salicylhydroxamic acid (SHAM). Physiol. Plant 116: 264–270.

    Google Scholar 

  • Goyal, A. and Tolbert, N.E. 1996. Association of glycolate oxidation with photosynthetic electron transport in plant and algal chloroplasts. Proc. Natl. Acad. Sci. USA 93: 3319–3324.

    Google Scholar 

  • Gross, W. (1999). Revision of comparative traits for the acidoand thermophilic red algae Cyanidium and Galdieria. In: J. Seckbach (Ed.), Enigmatic Microorganisms and Life in Extreme Environments, Kluwer, Dordrecht, pp. 437–446.

    Google Scholar 

  • Gross, W. 2000. Ecophysiology of algae living in highly acidic environments. Hydrobiology 433: 31–37.

    Google Scholar 

  • Gross, W. and Schnarrenberger, C. 1995a. Heterotrophic growth of 2 strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol. 36: 633–638.

    Google Scholar 

  • Gross, W. and Schnarrenberger, C. 1995b. Purification and characterization of a galactose-1-phosphate-UDP-glucose uridyltransferase from the red alga Galdieria sulphuraria. Eur. J. Biochem. 234: 258–263.

    Google Scholar 

  • Gross, W., Kuver, J., Tischendorf, G., Bouchaala, N. and Busch, W. 1998. Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur. J. Phycol. 33: 25–31.

    Google Scholar 

  • Gross, W., Oesterhelt, C., Tischendorf, G. and Lederer, F. 2002. Characterization of a non-thermophilic strain of the red algal genus Galdieria isolated from Soos (Czech Republic). Eur. J. Phycol. 37: 477–482.

    Google Scholar 

  • Heilmann, I., Schnarrenberger, C. and Gross, W. 1997. Mannose metabolizing enzymes from the red alga Galdieria sulphuraria. Phytochemistry 45: 903–906.

    Google Scholar 

  • Joyard, J., Grossmann, A., Bartlett, S.G., Douce, R. and Chua, N.H. 1982. Characterization of Envelope Membrane Polypeptides from Spinach Chloroplasts. J. Biol. Chem. 257: 1095–1101.

    Google Scholar 

  • Jung, S., Lowe, S.E., Hollingsworth, R.I. and Zeikus, J.G. 1993. Sarcina ventriculi synthesizes very long chain dicarboxylic acids in response to different forms of environmental stress. J. Biol. Chem. 268: 2828–2835.

    Google Scholar 

  • Jung, S., Zeikus, J.G. and Hollingsworth, R.I. 1994. A new family of very long chain alpha,omega-dicarboxylic acids is a major structural fatty acyl component of the membrane lipids of Thermoanaerobacter ethanolicus 39E. J. Lipid Res. 35: 1057–1065.

    Google Scholar 

  • Kammerer, B., Fischer, K., Hilpert, B., Schubert, S., Gutensohn, M., Weber, A. and Flügge, U.I. 1998. Molecular Characterization of a Carbon Transporter in Plastids from Heterotrophic Tissues: The Glucose6-Phosphate/Phosphate Antiporter. Plant Cell 10: 105–117.

    Google Scholar 

  • Knappe, S., Flügge, U.I. and Fischer, K. 2003. Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substratebinding site. Plant Physiol. 131: 1178–1190.

    Google Scholar 

  • Komatsu, H. and Chong, P.L. 1998. Low permeability of liposomal membranes composed of bipolar tetraether lipids from thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biochemistry 37: 107–115.

    Google Scholar 

  • Kremer, B.P. and Kirst, G.O. 1981. Biosynthesis of 2-O-Dglycerol-alpha-D-galactopyranoside (floridoside) in marine Rhodophyceae. Plant Sci. Lett. 23: 349–357.

    Google Scholar 

  • Lapidot, M., Raveh, D., Sivan, A., Arad, S. and Shapira, M. 2002. Stable chloroplast transformation of the unicellular red alga Porphyridium species. Plant Physiol. 129: 7–12.

    Google Scholar 

  • Linka, N., Hurka, H., Lang, F.B., Burger, G., Winkler, H.H., Stamme, C., Urbany, C., Seil, I., Kusch, J. and Neuhaus, H.E. 2003. Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene. 306: 27–35.

    Google Scholar 

  • Lluisma, A.O. and Ragan, M.A. 1998. Characterization of a galactose-1-phosphate uridylyltransferase gene from the marine red alga Gracilaria gracilis. Curr. Genet. 34: 112–119.

    Google Scholar 

  • Marquardt, J., Wans, S., Rhiel, E., Randolf, A. and Krumbein, W.E. 2000. Intron-exon structure and gene copy number of a gene encoding for a membrane-intrinsic light-harvesting polypeptide of the red alga Galdieria sulphuraria. Gene 255: 257–265.

    Google Scholar 

  • Martin, C. and Smith, A. 1995. Starch Biosynthesis. Plant Cell 7: 971–985.

    Google Scholar 

  • Matsuzaki, M., Misumi, O., Shin, I.T., Maruyama, S., Takahara, M., Miyagishima, S.Y., Mori, T., Nishida, K., Yagisawa, F., 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. and Kuroiwa, T. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657.

    Google Scholar 

  • Merola, A., Castaldo, R., De Luca, P., Gambardella, R., Musachio, A. and Taddei, R. 1981. Revision of Cyanidium caldarium. Three species of acidophylic algae. Giorn. Bot. Ital. 115: 189–195.

    Google Scholar 

  • Moreira, D., Lopezarchilla, A.I., Amils, R. and Marin, I. 1994. Characterization of 2 new thermoacidophilic microalgae- genome organization and comparison with Galdieria sulphuraria. FEMS Microbiol. Lett. 122: 109–114.

    Google Scholar 

  • Muravenko, O.V., Selyakh, I.O., Kononenko, N.V. and Stadnichuk, I.N. 2001. Chromosome numbers and nuclear DNA contents in the red microalgae Cyanidium caldarium and three Galdieria species. Eur. J. Phycol. 36: 227–232.

    Google Scholar 

  • Nagasaka, S., Nishizawa, N.K., Negishi, T., Satake, K., Mori, S. and Yoshimura, E. 2002. Novel iron-storage particles may play a role in aluminum tolerance of Cyanidium caldarium. Planta 215: 399–404.

    Google Scholar 

  • Niittyla, T., Messerli, G., Trevisan, M., Chen, J., Smith, A.M. and Zeeman, S.C. 2004. A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87–89.

    Google Scholar 

  • Oesterhelt, C. and Gross, W. 2002. Different sugar kinases are involved in the sugar sensing of Galdieria sulphuraria. Plant Physiol. 128: 291–299.

    Google Scholar 

  • Oesterhelt, C., Schnarrenberger, C. and Gross, W. 1996. Phosphomannomutase and phosphoglucomutase in the red alga Galdieria sulphuraria. Plant Sci. 121: 19–27.

    Google Scholar 

  • Oesterhelt, C., Schnarrenberger, C. and Gross, W. 1999. Characterization of a sugar/polyol uptake system in the red alga Galdieria sulphuraria. Eur. J. Phycol. 34: 271–277.

    Google Scholar 

  • Ohta, N., Matsuzaki, M., Misumi, O., Miyagishima, S.Y., Nozaki, H., Tanaka, K., Shin, I.T., Kohara, Y. and Kuroiwa, T. 2003. Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 10: 67–77.

    Google Scholar 

  • Okano, Y., Mizohata, E., Xie, Y., Matsumura, H., Sugawara, H., Inoue, T., Yokota, A. and Kai, Y. 2002. X-ray structure of Galdieria Rubisco complexed with one sulfate ion per active site. FEBS Lett. 527: 33–36.

    Google Scholar 

  • Oliveira, M.C. and Bhattacharya, D. 2000. Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. Am. J. Bot. 87: 482–492.

    Google Scholar 

  • Özcan, S., Dover, J. and Johnston, M. 1998. Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae. EMBO J 17: 2566–2573.

    Google Scholar 

  • Özcan, S., Dover, J., Rosenwald, A.G., Wolfl, S. and Johnston, M. 1996. Two glucose transporters in Saccharomyces cerevisiae are glucose sensors that generate a signal for induction of gene expression. Proc. Natl. Acad. Sci. USA 93: 12428–12432.

    Google Scholar 

  • Prosselkov, P.V., Gross, W., Igamberdiev, A.U. and Schnarrenberger, C. 1996. Purification and characterization of UDP-D-galactose 4-epimerase from the red alga Galdieria sulphuraria. Physiol. Plant 98: 753–758.

    Google Scholar 

  • Raetz, C.R. and Whitfield, C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71: 635–700.

    Google Scholar 

  • Rigano, C., Fuggi, A., Martino, D., Rigano, V. and Aliotta, G. 1976. Studies on utilization of 2-ketoglutarate, glutamate and other amino acids by the unicellular alga Cyanidium caldarium. Arch. Microbiol. 107: 133–138.

    Google Scholar 

  • Rothschild, L.J. and Mancinelli, R.L. 2001. Life in extreme environments. Nature 409: 1092–1101.

    Google Scholar 

  • Seckbach, J., Baker, F.A. and Shugarman, P.M. 1970. Algae thrive under pure CO2. Nature 227: 744–745.

    Google Scholar 

  • Seckbach, J. and Libby, W.F. 1970. Vegetative life on Venus? Or investigations with algae which grow under pure CO2 in hot acid media at elevated pressures. Space Life Sci. 2: 121–143.

    Google Scholar 

  • Smith, A.M. 1999. Making starch. Curr. Opin. Plant Biol. 2: 223–229.

    Google Scholar 

  • Smith, A.M., Denyer, K. and Martin, C. 1997. The synthesis of the starch granule. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 48: 67–87.

    Google Scholar 

  • Somerville, C., Browse, J., Jaworski, J.G., Ohlrogge, J.B. 2000. Lipids. In: B.B. Buchanan, W. Gruissem, and R.L. Jones (Eds.), Biochemistry and Molecular Biology of Plants, American Society of Plant Biologists, Rockville, MD, pp.456–527.

    Google Scholar 

  • Staehelin, L.A. 1968. Ultrastructural changes of the plasmalemma and the cell wall during the life cycle of Cyanidium caldarium. Proc. R. Soc. Lond. B. Biol. Sci. 171: 249–259.

    Google Scholar 

  • Sugawara, H., Yamamoto, H., Shibata, N., Inoue, T., Okada, S., Miyake, C., Yokota, A. and Kai, Y. 1999. Crystal structure of carboxylase reaction-oriented ribulose 1, 5-bisphosphate carboxylase/oxygenase from a thermophilic red alga, Galdieria partita. J. Biol. Chem. 274: 15655–15661.

    Google Scholar 

  • Takahashi, H., Takano, H., Yokoyama, A., Hara, Y., Kawano, S., Toh-e, A. and Kuroiwa, T. 1995. Isolation, characterization and chromosomal mapping of an actin gene from the primitive red alga Cyanidioschyzon merolae. Curr. Genet. 28: 484–490.

    Google Scholar 

  • Tansey, M.R. and Brock, T.D. 1972. The upper temperature limit for eukaryotic organisms. Proc Natl Acad Sci USA 69: 2426–2428.

    Google Scholar 

  • Uemura, K., Anwaruzzaman, Miyachi, S. and Yokota, A. 1997. Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. Biochem. Biophys. Res. Commun. 233: 568–571.

    Google Scholar 

  • Urbach, W. and Gimmler, H. 1968. Stimulation of glycollate excretion of algae by disalicylidenepropanediamine and hydroxypyridinemethanesulfonate. Z. Naturforsch. B 23: 1282–1283.

    Google Scholar 

  • Veramendi, J., Roessner, U., Renz, A., Willmitzer, L. and Trethewey, R.N. 1999. antisense repression of hexokinase 1 leads to an overaccumulation of starch in leaves of transgenic potato plants but not to significant changes in tuber carbohydrate metabolism. Plant Physiol. 121: 123–134.

    Google Scholar 

  • Viola, R., Nyvall, P. and Pedersen, M. 2001. The unique features of starch metabolism in red algae. Proc. Roy. Soc. Lond. B 268: 1417–1422.

    Google Scholar 

  • Weber, A., Servaites, J.C., Geiger, D.R., Kofler, H., Hille, D., Gröner, F., Hebbeker, U. and Flügge, U.I. 2000. Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787–801.

    Google Scholar 

  • Weise, S.E., Weber, A.P. and Sharkey, T.D. 2004. Maltose is the major form of carbon exported from the chloroplast at night. Planta 218: 474–482.

    Google Scholar 

  • Wiese A., Gröner, F., Sonnewald, U., Deppner, H., Lerchl, J., Hebbeker, U., Flügge, U.I., and Weber, A. 1999. Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett 461: 13–18.

    Google Scholar 

  • Wendl, M.C., Marra, M.A., Hillier, L.W., Chinwalla, A.T., Wilson, R.K. and Waterston, R.H. 2001. Theories and applications for sequencing randomly selected clones. Genome Res 11: 274–280.

    Google Scholar 

  • Williams, L.E., Lemoine, R., and Sauer, N. 2000. Sugar transporters in higher plants - A diversity of roles and complex regulation. Trends Plant Sci. 5: 283–290.

    Google Scholar 

  • Yoshimura, E., Nagasaka, S., Satake, K., and Mori, S. 2000. Mechanism of aluminium tolerance in Cyanidium caldarium. Hydrobiology 433: 57–60.

    Google Scholar 

  • Yoshimura, E., Nagasaka, S., Sato, Y., Satake, K. and Mori, S. 1999. Extraordinary high aluminium tolerance of the acidophilic thermophilic alga, Cyanidium caldarium. Soil Sci. Plant Nutrit. 45: 721–724.

    Google Scholar 

  • Yu, S.K., Blennow, A., Bojko, M., Madsen, F., Olsen, C.E., and Engelsen, S.B. 2002. Physicochemical characterization of floridean starch of red algae. Starch-Stärke 54: 66–74.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Biology, Michigan State University, USA

    Andreas Weber, Andrea Bräutigam, Lori Imboden, Inga Krassovskaya, Nicole Linka, Julia Truchina, Jörg Schneidereit, Hildegard Voll, Lars Voll, Marc Zimmermann, Aziz Jamai, Wayne Riekhof, Bin Yu, R. Garavito & Christoph Benning

  2. Institut für Biochemie und Biologie, Universität Potsdam, Germany

    Christine Oesterhelt

  3. Institut für Pflanzenphysiologie und Mikrobiologie, Freie Universität Berlin, Königin-Luise-Str, Germany

    Wolfgang Gross

  4. MSU-DOE Plant Research Laboratory, USA

    Wayne Riekhof

Authors
  1. Andreas Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christine Oesterhelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wolfgang Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea Bräutigam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lori Imboden
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Inga Krassovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nicole Linka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Julia Truchina
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jörg Schneidereit
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hildegard Voll
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lars Voll
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Marc Zimmermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Aziz Jamai
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Wayne Riekhof
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Bin Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. R. Garavito
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Christoph Benning
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weber, A., Oesterhelt, C., Gross, W. et al. EST-analysis of the thermo-acidophilic red microalga Galdieriasulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55, 17–32 (2004). https://doi.org/10.1007/s11103-004-0376-y

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-0376-y

Search

Navigation