Carbon Fixation in Diatoms

  • Yusuke MatsudaEmail author
  • Peter G. Kroth
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)


Diatoms are unicellular photoautotrophic algae and very successful primary producers in the oceans. Their high primary productivity is probably sustained by their high adaptability and a uniquely arranged metabolism. Diatom belongs to the Chromista, a large eukaryotic group, which has evolved by multiple endosymbiotic steps. As a result, diatoms possess a plastids with four membranes together with complicated translocation systems to transport proteins and metabolites including inorganic substances into and out of the plastids. In addition to the occurrence of potential plasma-membrane transporters, there are numerous carbonic anhydrases (CAs) within the matrix of the layered plastidic membranes, strongly suggesting large interconversion activity between CO2 and HCO3 within the chloroplast envelope as a part of a CO2-concentrating mechanism (CCM). In diatoms also the Calvin cycle and its adjacent metabolism reveal unique characteristics as, for instance, ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) activase, the plastidic sedoheptulose-1,7-bisphosphatase (SBPase), and the plastidic oxidative pentose phosphate pathway (OPP) are absent. Furthermore, the Calvin cycle metabolism in diatoms is not under the strict redox control by the thioredoxin (Trx) system. Instead, a CO2-supplying system in the pyrenoid shows CA activities which are probably regulated by chloroplastic Trxs. Pyrenoidal CAs are also regulated on the transcriptional level by CO2 concentrations via cAMP as a second messenger, suggesting an intense control system of CO2 acquisition in response to CO2 availability. The photorespiratory carbon oxidation cycle (PCOC) is the major pathway to recycle phosphoglycolate in diatoms although this process might not be involved in recycling of 3-phosphoglycerate but instead produces glycine and serine. In this review we focus on recent experimental data together with supportive genome information of CO2 acquisition and fixation systems primarily in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana.


Carbonic Anhydrase Dissolve Inorganic Carbon Calvin Cycle Marine Diatom Centric Diatom 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



– Adenylyl cyclase;


– Carbonic anhydrase;


– CO2-concentrating mechanism;


– Dissolved-inorganic carbon;


– Fructose-1,6-bisphosphate aldolase;


– Fructose-1,6-bisphosphatase;


– Ferredoxin;


– Horizontal gene transfer;


– Low-CO2-inducible proteins;


– Nucleotide translocators;


– Oxidative pentose phosphate pathway;


– Photorespiratory carbon oxidation cycle;


– Phosphoenol pyruvate carboxykinase;


– Pyruvate orthophosphate dikinase;


– Ribulose-1,5-bisphosphate carboxylase/oxygenase;


– Solute carrier;


– Thioredoxin



This work was supported by Grant-in-Aid for Scientific Research B (grant no. 24310015 to Y. M.), by Grant-in-Aid for Challenging Exploratory Research (grant no. 24651119 to Y. M.) from the Japan Society for the Promotion of Science (JSPS), by MEXT-Supported Program for the Strategic Research Foundation at Private Universities (2010–2014), by the Program for Research on Halophilic Organism of the Salt Science Research Foundation (grant no. 06B02 to Y. M.), and by the Steel Industry Foundation for the Advancement of Environmental Protection Technology to Y. M. PGK is grateful for financial support by the German Research Foundation (DFG), grant KR1661/7-1, the German Israeli Foundation (GIF), the University of Konstanz, and is thankful to A. Gruber and J. Hentschel for providing an unpublished electron micrograph.


  1. Allen AE, Dupont CL, Obornik M, Horák A, Nunes-Nesi A, McCrow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473:203–207PubMedGoogle Scholar
  2. Allen AE, Moustafa A, Montsant A, Eckert A, Kroth PG, Bowler C (2012) Evolution and functional diversification of fructose bisphosphate aldolase genes in photosynthetic marine diatoms. Mol Biol Evol 29:367–379PubMedCentralPubMedGoogle Scholar
  3. Alterio V, Langella E, Viparelli F, Vullo D, Ascione G, Dathan NA, Morel FMM, Supuran CT, De Simone G, Monti SM (2012) Structural and inhibition insights into carbonic anhydrase CDCA1 from the marine diatom Thalassiosira weissflogii. Biochimie 94:1232–1241PubMedGoogle Scholar
  4. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86PubMedGoogle Scholar
  5. Arsova B, Hoja U, Wimmelbacher M, Greiner E, Üstün S, Melzer M, Petersen K, Lein W, Börnke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515PubMedCentralPubMedGoogle Scholar
  6. Ast M, Gruber A, Schmitz-Esser S, Neuhaus HE, Kroth PG, Horn M, Haferkamp I (2009) Diatom plastids depend on nucleotide import from the cytosol. Proc Natl Acad Sci U S A 106:3621–3626PubMedCentralPubMedGoogle Scholar
  7. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of RubisCO, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76:1052–1071Google Scholar
  8. Badger MR, Hanson D, Price GD (2002) Evolution and diversity of CO2-concentrating mechanisms in cyanobacteria. Funct Plant Biol 29:183–194Google Scholar
  9. Balmer Y, Koller A, del Val G, Manieri W, Schürmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci U S A 100:370–375PubMedCentralPubMedGoogle Scholar
  10. Borkhsenious ON, Mason CB, Moroney JV (1998) The intracellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. Plant Physiol 116:1585–1591PubMedCentralPubMedGoogle Scholar
  11. Bosco MB, Aleanzi MC, Iglesias AA (2012) Plastidic phosphoglycerate kinase from Phaeodactylum tricornutum: on the critical role of cysteine residues for the enzyme function. Protist 163:188–203PubMedGoogle Scholar
  12. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jezequel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van de Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244PubMedGoogle Scholar
  13. Bozzo GG, Colman B (2000) The induction of inorganic carbon transport and external carbonic anhydrase in Chlamydomonas reinhardtii is regulated by external CO2 concentration. Plant Cell Environ 23:1137–1144Google Scholar
  14. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220PubMedGoogle Scholar
  15. Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E (2010) Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem 285:6848–6856PubMedCentralPubMedGoogle Scholar
  16. Burkhardt S, Amoroso G, Riebesell U, Sültemeyer D (2001) CO2 and HCO3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46:1378–1391Google Scholar
  17. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366PubMedGoogle Scholar
  18. Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5:174–182PubMedGoogle Scholar
  19. Chaal BK, Ishida K, Green BR (2003) A thylakoidal processing peptidase from the heterokont alga Heterosigma akashiwo. Plant Mol Biol 52:463–472PubMedGoogle Scholar
  20. Chan CX, Reyes-Prieto A, Bhattacharya D (2011) Red and green algal origin of diatom membrane transporter: insights into environmental adaptation and cell evolution. PLoS One 6:e29138PubMedCentralPubMedGoogle Scholar
  21. Chan CX, Bhattacharya D, Reyes-Prieto A (2012) Endosymbiotic and horizontal gene transfer in microbial eukaryotes: impacts on cell evolution and the tree of life. Mob Genet Elem 2:101–105Google Scholar
  22. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625–628PubMedGoogle Scholar
  23. Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M (2003) The Arabidop plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278:23747–23752PubMedGoogle Scholar
  24. Colman B, Rotatore C (1995) Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant Cell Environ 18:919–924Google Scholar
  25. Cox EH, McLendon GL, Morel FMM, Lane TW, Prince RC, Pickering IJ, George GN (2000) The active site structure of Thalassiosira weissflogii carbonic anhydrase 1. Biochemistry 39:12128–12130PubMedGoogle Scholar
  26. Danson JS, Huertas IE, Colman B (2004) Source of inorganic carbon for photosynthesis in two marine dinoflagellates. J Phycol 40:285–292Google Scholar
  27. De Riso V, Raniello R, Maumus F, Rogato A, Bowler C, Falciatore A (2009) Gene silencing in the marine diatom Phaeodactylum tricornutum. Nucl Acids Res 37:e96PubMedCentralPubMedGoogle Scholar
  28. Delwiche CF, Palmer JD (1997) The origin of plastids and their spread via secondary symbiosis. Plant Syst Evol 11:53–86Google Scholar
  29. Deschamps P, Moreira D (2012) Reevaluating the green contribution to diatom genomes. Genome Biol Evol 4:683–688PubMedGoogle Scholar
  30. Dionisio-Sese ML, Fukuzawa H, Miyachi S (1990) Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 94:1103–1110PubMedCentralPubMedGoogle Scholar
  31. Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC (2008) CO2 fixation kinetics of Halothiobacillus neapolitanus mutant carboxysomes lacking carbonic anhydrase suggest the shell acts as a diffusional barrier for CO2. J Biol Chem 283:10377–10384PubMedGoogle Scholar
  32. Duanmu D, Spalding MH (2011) Insertional suppressors of Chlamydomonas reinhardtii that restore growth of air-dier lcib mutants in low CO2. Photosynth Res 109:123–132PubMedGoogle Scholar
  33. Eisenhut M, Kahlon S, Hasse D, Ewald R, Lieman-Hurwitz J, Ogawa T, Ruth W, Bauwe H, Kaplan A, Hagemann M (2006) The plant-like C2 glycolate cycle and the bacterial like glycerate pathway cooperate in phophoglycolate metabolism in cyanobacteria. Plant Physiol 142:333–342PubMedCentralPubMedGoogle Scholar
  34. Fabris M, Matthijs M, Rombauts S, Vyverman W, Goossens A, Baart GJE (2012) The metabolic blueprint of Phaeodactylum tricornutum reveals a eukaryotic Entner–Doudoroff glycolytic pathway. Plant J 70:1004–1014PubMedGoogle Scholar
  35. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  36. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hoegberg P, Linder S, Mackenzie FT, III Moore B, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W (2000) The global carbon cycle: a test of our knowledge of Earth as a system. Science 290:291–296PubMedGoogle Scholar
  37. Fukuzawa H, Suzuki E, Komukai Y, Miyachi S (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Proc Natl Acad Sci U S A 89:4437–4441PubMedCentralPubMedGoogle Scholar
  38. Fukuzawa H, Miura K, Ishizaki K, Kucho KI, Saito T, Kohinata T, Ohyama K (2001) Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proc Natl Acad Sci U S A 98:5347–5352PubMedCentralPubMedGoogle Scholar
  39. Funke RP, Kovar JL, Weeks DP (1997) Intracellular carbonic anhydrase is essential to photosynthesis in Chlamydomonas reinhardtii at atmospheric levels of CO2. Demonstration via genomic complementation of the high-CO2-requiring mutant ca-1. Plant Physiol 114:237–244PubMedCentralPubMedGoogle Scholar
  40. Genkov T, Meyer M, Griffiths H, Spreitzer RJ (2010) Functional hybrid RubisCO enzymes with plant small subunits and algal large subunits: engineered rbcS cDNA for expression in Chlamydomonas. J Biol Chem 285:19833–19841PubMedCentralPubMedGoogle Scholar
  41. Giordano M, Norici A, Forssen M, Eriksson M, Raven JA (2003) An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132:2126–2134PubMedCentralPubMedGoogle Scholar
  42. Goyet C, Poisson A (1989) New determination of carbonic acid dissociation constants in seawater as a function of temperature and salinity. Deep-Sea Res 36:1635–1654Google Scholar
  43. Gruber A, Vugrinec S, Hempel F, Gould SB, Maier UG, Kroth PG (2007) Protein targeting into complex diatom plastids depends on the signal peptide’s cleavage site within the bipartite presequence. Plant Mol Biol 64:519–530PubMedGoogle Scholar
  44. Gruber A, Weber T, Bártulos CR, Vugrinec S, Kroth PG (2009) Intracellular distribution of the reductive and oxidative pentase phosphate pathways in two diatoms. J Basic Microbiol 49:58–72PubMedGoogle Scholar
  45. Haimovich-Dayan M, Garfinkel N, Ewe D, Marcus Y, Gruber A, Wagner H, Kroth PG, Kaplan A (2013) The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. New Phytol 197:177–185Google Scholar
  46. Hammer A, Hodgson DR, Cann MJ (2006) Regulation of prokaryotic adenylyl cyclases by CO2. Biochem J 396:215–218PubMedCentralPubMedGoogle Scholar
  47. Harada H, Matsuda Y (2005) Identification and characterization of a new carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Can J Bot 83:909–916Google Scholar
  48. Harada H, Nakatsuma D, Ishida M, Matsuda Y (2005) Regulation of the expression of intracellular β-carbonic anhydrase in response to CO2 and light in the marine diatom Phaeodactylum tricornutum. Plant Physiol 139:1041–1050PubMedCentralPubMedGoogle Scholar
  49. Harada H, Nakajima K, Sakaue K, Matsuda Y (2006) CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiol 142:1318–1328PubMedCentralPubMedGoogle Scholar
  50. Holdsworth RH (1971) The isolation and partial characterization of the pyrenoid protein of Eremosphaera viridis. J Cell Biol 51:499–513PubMedCentralPubMedGoogle Scholar
  51. Hopkinson BM (2013) A chloroplast pump model for the CO2 concentrating mechanism in the diatom Phaeodactylum tricornutum. Photosynth Res. doi: 10.1007/s11120-013-9954-7 PubMedGoogle Scholar
  52. Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Natl Acad Sci USA 108:3830–3837PubMedCentralPubMedGoogle Scholar
  53. Jenks A, Gibbs SP (2000) Immunolocalization and distribution of form II RubisCO in the pyrenoid and chloroplast stroma of Amphidinium carterae and form I RubisCO in the symbiont-derived plastids of Perinidium foliaceum (Dinophyceae). J Phycol 36:127–138Google Scholar
  54. John-Mckay ME, Colman B (1997) Variation in the occurrence of external carbonic anhydrase among strains of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 33:988–990Google Scholar
  55. Johnston AM, Raven JA (1996) Inorganic carbon accumulation by the marine diatom Phaeodactylum tricornutum. Eur J Phycol 31:285–290Google Scholar
  56. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G (1998) A novel α-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17:1208–1216PubMedCentralPubMedGoogle Scholar
  57. Kerfeld CA, Sawaya MR, Tanaka S, Nguyen CV, Phillips M, Beeby M, Yeates TO (2005) Protein structures forming the shell of primitive bacterial organelles. Science 309:936–938PubMedGoogle Scholar
  58. Kikutani S, Tanaka R, Yamazaki Y, Hara S, Hisabori T, Kroth PG, Matsuda Y (2012) Redox regulation of carbonic anhydrases via thioredoxin in the chloroplast of the marine diatom Phaeodactylum tricornutum. J Biol Chem 287:20689–20700PubMedCentralPubMedGoogle Scholar
  59. Kilian O, Kroth PG (2004) Presequence acquisition during secondary endocytobiosis and the possible role of introns. J Mol Evol 58:712–721PubMedGoogle Scholar
  60. Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41:175–183PubMedGoogle Scholar
  61. Kitao Y, Matsuda Y (2009) Formation of macromolecular complexes of carbonic anhydrases in the chloroplast of a marine diatom by the action of the C-terminal helix. Biochem J 419:681–688PubMedGoogle Scholar
  62. Kitao Y, Harada H, Matsuda Y (2008) Localization and targeting mechanisms of two chloroplastic β-carbonic anhydrases in the marine diatom Phaeodactylum tricornutum. Physiol Plant 133:68–77PubMedGoogle Scholar
  63. Klengel T, Liang WJ, Chaloupka J, Ruoff C, Schröppel K, Naglik JR, Eckert SE, Mogensen EG, Haynes K, Tuite MF, Levin LR, Buck J, Mühlschlegel FA (2005) Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15:2021–2026PubMedCentralPubMedGoogle Scholar
  64. Kohinata T, Nishino H, Fukuzawa H (2008) Significance of zinc in a regulatory protein, CCM1, which regulates the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol 49:273–283PubMedGoogle Scholar
  65. Kooistra WHCF, Gersonde R, Medlin LK, Mann DG (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea. Academic Press, Burlington, pp 207–249Google Scholar
  66. Korb RE, Saville PJ, Johnston AM, Raven JA (1997) Sources of inorganic carbon for photosynthesis by three species of marine diatom. J Phycol 33:433–440Google Scholar
  67. Kozaki A, Takeba G (1996) Photoinhibition protects C3 plants from photooxidation. Nature 384:557–560Google Scholar
  68. Kroth PG (2002) Protein transport into secondary plastids and the evolution of primary and secondary plastids. Int Rev Cytol 221:191–255PubMedGoogle Scholar
  69. 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:e1426PubMedCentralPubMedGoogle Scholar
  70. Kuchitsu K, Tsuzuki M, Miyachi S (1988) Characterization of the pyrenoid isolated from unicellular green alga Chlamydomonas reinhardtii: particulate from RubisCO protein. Protoplasma 144:17–24Google Scholar
  71. Kuchitsu K, Tsuzuki M, Miyachi S (1991) Polypeptide composition and enzyme activities of the pyrenoid and its regulation by CO2 concentration in unicellular green algae. Can J Bot 69:1062–1069Google Scholar
  72. Kucho K, Ohyama K, Fukuzawa H (1999) CO2-responsive transcriptional regulation of CAH1 encoding carbonic anhydrase is mediated by enhancerand silencer regions in Chlamydomonas reinhardtii. Plant Physiol 121:1329–1337PubMedCentralPubMedGoogle Scholar
  73. Lacoste-Royal G, Gibbs SP (1987) Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase in the pyrenoid and thylakoid region of the chloroplast of Chlamydomonas reinhardtii. Plant Physiol 83:602–606PubMedCentralPubMedGoogle Scholar
  74. Lane TW, Morel FMM (2000) A biological function for cadmium in marine diatoms. Proc Natl Acad Sci U S A 97:4627–4631PubMedCentralPubMedGoogle Scholar
  75. Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM (2005) A cadmium enzyme from marine diatom. Nature 435:42PubMedGoogle Scholar
  76. Lang M, Kroth PG (2001) Diatom fucoxanthin chlorophyll a/c-binding protein (FCP) and land plant light-harvesting proteins use a similar pathway for thylakoid membrane insertion. J Biol Chem 276:7985–7991PubMedGoogle Scholar
  77. Lang M, Apt KE, Kroth PG (1998) Protein transport into “complex” diatom plastids utilizes two different targeting signals. J Biol Chem 273:30973–30978PubMedGoogle Scholar
  78. Lapointe M, Mackenzie TDB, Morse D (2008) An external δ-carbonic anhydrase in a free-living marine dinoflagellate may circumvent diffusion-limited carbon acquisition. Plant Physiol 147:1427–1436PubMedCentralPubMedGoogle Scholar
  79. Lavaud J, Materna AC, Sturm S, Vugrinec S, Kroth PG (2012) Silencing of the violaxanthin de-epoxidase gene in the diatom Phaeodactylum tricornutum reduces diatoxanthin synthesis and non-photochemical quenching. PLoS One 7:e36806PubMedCentralPubMedGoogle Scholar
  80. Lee RBY, Smith JAC, Rickaby REM (2013) Cloning, expression and characterization of the δ-carbonic anhydrase of Thalassiosira weissflogii (Bacillariophyceae). J Phycol 49:170–177Google Scholar
  81. Lemaire SD, Miginiac-Maslow M (2004) The thioredoxin superfamily in Chlamydomonas reinhardtii. Photosynth Res 82:203–220PubMedGoogle Scholar
  82. Lemaire SD, Collin V, Keryer E, Quesada A, Miginiac-Masalow M (2003) Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Lett 543:87–92PubMedGoogle Scholar
  83. Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 101:7475–7480PubMedCentralPubMedGoogle Scholar
  84. Liaud MF, Lichtlé C, Apt K, Martin W, Cerff R (2000) Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol Biol Evol 17:213–223PubMedGoogle Scholar
  85. Long BM, Badger MR, Whitney SM, Price GD (2007) Analysis of carboxysomes from Synechococcus PCC7942 reveals multiuple RubisCO complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282:29323–29335PubMedGoogle Scholar
  86. Lopez-Ruiz A, Verbelen JP, Roldan JM, Diez J (1985) Nitrate reductase of green algae is located in the pyrenoid. Plant Physiol 79:1006–1010PubMedCentralPubMedGoogle Scholar
  87. Maeda S, Badger MR, Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium Synechococcus sp. PCC7942. Mol Microbiol 43:425–436PubMedGoogle Scholar
  88. Marcus Y, Harel E, Kaplan A (1983) Adaptation of the cyanobacterium Anabaena variabilis to low CO2 concentration in their environment. Plant Physiol 71:208–210PubMedCentralPubMedGoogle Scholar
  89. Matsuda Y, Colman B (1995a) Induction of CO2 and bicarbonate transport in green alga Chlorella ellipsoidea. Time course of induction of two systems. Plant Physiol 108:247–252PubMedCentralPubMedGoogle Scholar
  90. Matsuda Y, Colman B (1995b) Induction of CO2 and bicarbonate transport in green alga Chlorella ellipsoidea. Evidence for induction in response to external CO2 concentration. Plant Physiol 108:253–260PubMedCentralPubMedGoogle Scholar
  91. Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom Phaeodactylum tricornutum. Plant Cell Environ 24:611–620Google Scholar
  92. Matsuda Y, Satoh K, Harada H, Satoh D, Hiraoka Y, Hara T (2002) Regulation of the expressions of HCO3 uptake and intracellular carbonic anhydrase in response to CO2 concentrating in the marine diatom Phaeodactylum sp. Funct Plant Biol 29:279–287Google Scholar
  93. Matsuda Y, Nakajima K, Tachibana M (2011) Recent progresses on the genetic basis of the regulation of CO2 acquisition systems in response to CO2 concentration. Photosynth Res 109:191–203PubMedGoogle Scholar
  94. Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S, 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 merolae10D. Nature 428:653–657PubMedGoogle Scholar
  95. Mayo WP, Williams TG, Birch DG, Turpin DH (1986) Photosynthetic adaptation by Synechococcus leopoliensis in response to exogenous dissolved inorganic carbon. Plant Physiol 80:1038–1040PubMedCentralPubMedGoogle Scholar
  96. McGinn PJ, Morel FMM (2008) Expression and inhibition of the carboxylating and decarboxylating enzymes in the photosynthetic C4 pathway of marine diatoms. Plant Physiol 146:300–309PubMedCentralPubMedGoogle Scholar
  97. McKay RML, Gibbs SP (1989) Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in light-limited and light-saturated cells of Chlorella pyrenoidosa. Protoplasma 149:31–37Google Scholar
  98. McKay RML, Gibbs SP (1990) Phycoerythrin is absent from the pyrenoid of Porphyridium cruentum: photosynthetic implications. Planta 180:249–256PubMedGoogle Scholar
  99. McKay RML, Gibbs SP, Vaughn KC (1991) RubisCO activase is present in the pyrenoid of green algae. Protoplasma 162:38–45Google Scholar
  100. Mestres-Ortega D, Meyer Y (1999) The Arabidopsis thaliana genome encodes at least four thioredoxins m and a new prokaryotic-like thioredoxin. Gene 240:307–316PubMedGoogle Scholar
  101. Meyer Y, Buchanan BB, Vignols F, Reichheld JP (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367PubMedGoogle Scholar
  102. Michels AK, Wedel N, Kroth PG (2005) Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway. Plant Physiol 137:911–920PubMedCentralPubMedGoogle Scholar
  103. Milligan AJ, Morel FMM (2002) A proton buffering role for silica in diatoms. Science 297:1848–1850PubMedGoogle Scholar
  104. Mitchell C, Beardall J (1996) Inorganic carbon uptake by an Antarctic sea-ice diatom, Nitzschia frigida. Polar Biol 16:95–99Google Scholar
  105. Mitra M, Lato SM, Ynalvez RA, Xiao Y, Moroney JV (2004) Identification of a new chloroplast carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 135:173–182PubMedCentralPubMedGoogle Scholar
  106. Miura K, Kohinata T, Yoshioka S, Ohyama K, Fukuzawa H (2002) Regulation of a carbon concentrating mechanism through CCM1 in Chlamydomonas reinhardtii. Funct Plant Biol 29:211–219Google Scholar
  107. Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT, Ohyama K, Fukuzawa H (2004) Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 135:1595–1607PubMedCentralPubMedGoogle Scholar
  108. Montsant A, Jabbari K, Maheswari U, Bowler C (2005) Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Physiol 137:500–513PubMedCentralPubMedGoogle Scholar
  109. Morita E, Abe T, Tsuzuki M, Fujiwara S, Sato N, Hirata A, Sonoike K, Nozaki H (1998) Presence of the CO2-concentraitng mechanism in some species of the pyrenoid-less free-living algal genus Chloromonas (Volvocales, Chlorophyta). Planta 204:269–276PubMedGoogle Scholar
  110. Motohashi K, Kondoh A, Stumpp MT, Hisabori T (2001) Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci U S A 98:11224–11229PubMedCentralPubMedGoogle Scholar
  111. Moustafa A, Reyes-Prieto A, Bhattacharya D (2008) Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastids functions. PLoS One 3:e2205PubMedCentralPubMedGoogle Scholar
  112. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726PubMedGoogle Scholar
  113. Mueller-Cajar O, Stotz M, Wendler P, Hartl FU, Bracher A, Hayer-Hartl M (2011) Structure and function of the AAA+ protein CbbX, a red-type RubisCO activase. Nature 479:194–199PubMedGoogle Scholar
  114. Nakajima K, Tanaka A, Matsuda Y (2013) SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc Natl Acad Sci USA 110(5):1767–1772PubMedCentralPubMedGoogle Scholar
  115. Nimer NA, Brownlee C, Merrett MJ (1999) Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiol 120:105–112PubMedCentralPubMedGoogle Scholar
  116. Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda S, Omata T (2008) Mechanism of low CO2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. Mol Microbiol 68:98–109PubMedGoogle Scholar
  117. Norton TA, Melkonian M, Anderson RA (1996) Algal biodiversity. Phycologia 35:308–326Google Scholar
  118. Ohnishi N, Mukherjee B, Tsujikawa T, Yanase M, Nakano H, Moroney JV, Fukuzawa H (2010) Expression of a low CO2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22:3105–3117PubMedCentralPubMedGoogle Scholar
  119. Ohno N, Inoue T, Yamashiki R, Nakajima K, Kitahara Y, Ishibashi M, Matsuda Y (2012) CO2-cAMP-responsive cis-elements targeted by a transcription factor with CREB/ATF-like basic zipper domain in the marine diatom Phaeodactylum tricornutum. Plant Physiol 158:499–513PubMedCentralPubMedGoogle Scholar
  120. Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci U S A 96:13571–13576PubMedCentralPubMedGoogle Scholar
  121. Omata T, Gohta S, Takahashi Y, Harano Y, Maeda S (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183:1891–1898PubMedCentralPubMedGoogle Scholar
  122. Osafune T, Yokota A, Sumida S, Hase E (1990) Immunogold localization of ribulose-1,5-bisphosphate carboxylase with reference to pyrenoid morphology in chloroplasts of synchronized Euglena gracilis cells. Plant Physiol 92:802–808PubMedCentralPubMedGoogle Scholar
  123. Oudot-Le Secq MP, Green BR (2011) Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene 476:20–26PubMedGoogle Scholar
  124. Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BV (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics 277:427–439PubMedGoogle Scholar
  125. Parker MS, Armbrust EV, Piovia-Scott J, Keil RG (2004) Induction of photorespiration by light in the centric diatom Thalassiosira weissflogii (Bacillariophyceae): molecular characterization and physiological consequences. J Phycol 40:557–567Google Scholar
  126. Patel BN, Merrett MJ (1986) Inorganic-carbon uptake by the marine diatom Phaeodactylum tricornutum. Planta 169:222–227PubMedGoogle Scholar
  127. Paul JS, Volcani BE (1974) Photorespiration in diatoms I. The oxidation of glycolic acid in Thalassiosira pseudonana. Arch Microbiol 101:115–120PubMedGoogle Scholar
  128. Paul JS, Volcani BE (1976) Photorespiration in diatoms IV. Two pathways of glycolate metabolism in synchronized cultures of Cylindrotheca fuciformis. Arch Microbiol 110:247–252PubMedGoogle Scholar
  129. Poulsen N, Chesley PM, Kröger N (2006) Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 42:1059–1065Google Scholar
  130. Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci U S A 101:18228–18233PubMedCentralPubMedGoogle Scholar
  131. Prihoda J, Tanaka A, de Paula WBM, Allen JF, Tirichine L, Bowler C (2012) Chloroplast-mitochondria cross-talk in diatoms. J Exp Bot 63:1543–1557PubMedGoogle Scholar
  132. Pronina NA, Semenenko VE (1984) Localization of membrane bound and soluble forms of carbonic anhydrase in the Chlorella cell. Fiziol Rast (Moscow) 31:241–251Google Scholar
  133. Qiu H, Yoon HS, Bhattacharya D (2013) Algal endosymbionts as vectors of horizontal gene transfer in photosynthetic eukaryotes. Front Plant Sci 19:366Google Scholar
  134. Ratti S, Giordano M, Morse D (2007) CO2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J Phycol 43:693–701Google Scholar
  135. Raven JA (1997) CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ 20:147–154Google Scholar
  136. Reinfelder JR, Kraepiel AML, Morel FMM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407:996–999PubMedGoogle Scholar
  137. Reinfelder JR, Milligan AJ, Morel FMM (2004) The Role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135:2106–2111PubMedCentralPubMedGoogle Scholar
  138. Roberts SB, Lane TW, Morel FMM (1997) Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 33:845–850Google Scholar
  139. Roberts K, Granum E, Leegood RC, Raven JA (2007a) Carbon acquisition by diatoms. Photosynth Res 93:79–88PubMedGoogle Scholar
  140. Roberts K, Granum E, Leegood RC, Raven JA (2007b) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol 145:230–235PubMedCentralPubMedGoogle Scholar
  141. Rogers M, Keeling PJ (2004) Lateral transfer and recompartmentalization of Calvin cycle enzymes of plants and algae. J Mol Evol 58:367–375PubMedGoogle Scholar
  142. Rost B, Riebesell U, Burkhardt S (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67Google Scholar
  143. Rotatore C, Colman B, Kuzuma M (1995) The active uptake of carbon dioxide by the marine diatom Phaeodactylum triconrutum and Cyclotella sp. Plant Cell Environ 18:913–918Google Scholar
  144. Sakaguchi T, Nakajima K, Matsuda Y (2011) Identification of the UMP stnthase gene by establishment of uracil auxotrophic mutants and the phenotypic complementation system in the marine diatom Phaeodactylum tricornutum. Plant Physiol 156:78–89PubMedCentralPubMedGoogle Scholar
  145. Samukawa M, Shen C, Hopkinson BM, Matsuda Y (2014) Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosynth Res. doi: 10.1007/s11120-014-9967-x PubMedGoogle Scholar
  146. Satoh D, HiraokaY, Colman B, Matsuda Y (2001) Physiological and molecular biological characterization of intracellular carbonic anhydrase from the marine diatom Phaeodactylum tricornutum. Plant Physiol 126:1459–1470Google Scholar
  147. Sawaya MR, Cannon GC, Heinhorst S, Tanaka S, Williams EB, Yeates TO, Kerfeld CA (2006) The structure of β-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J Biol Chem 281:7546–7455PubMedGoogle Scholar
  148. Schuerman P, Jacquot JP (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51:371–400Google Scholar
  149. Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277:18658–18664PubMedGoogle Scholar
  150. Sims PA, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45:361–402Google Scholar
  151. So AK, Cot SSW, Espie GS (2002) Characterization of the C-terminal extension of carboxysomal carbonic anhydrase from Synechocystis sp PCC6803. Funct Plant Biol 29:183–194Google Scholar
  152. So AK, Espie GS, Williams EB, Shively JM, Heinhorst S, Cannon GC (2004) A novel evolutionary lineage of carbonic anhydrase (ε class) is a component of the carboxysome shell. J Bacteriol 186:623–630PubMedCentralPubMedGoogle Scholar
  153. Sommer MS, Gould SB, Lehmann P, Gruber A, Przyborski JM, Maier UG (2007) Der1-mediated preprotein import into the periplastid compartoment of chromalveolates? Mol Biol Evol 24:918–928PubMedGoogle Scholar
  154. Soto AR, Zheng H, Shoemaker D, Rodriguez J, Read BA, Wahlund TM (2006) Identification and preliminary characterization of two cDNAs encoding unique carbonic anhydrases from the marine alga Emiliania huxleyi. Appl Environ Microbiol 72:5500–5511PubMedCentralPubMedGoogle Scholar
  155. Spalding MH, Spreitzer RJ, Ogren WL (1983) Carbonic anhydrase-deficient mutant of Chlamydomonas reinhardtii requires elevated carbon-dioxide concentration for photoautotrophic growth. Plant Physiol 73:268–272PubMedCentralPubMedGoogle Scholar
  156. Sueltemeyer DF, Fock HP, Canvin DT (1991) Active uptake of inorganic carbon by Chlamydomonas reinhardtii: evidence for simultaneous transport of HCO3 and CO2 and characterization of active CO2 transport. Can J Bot 69:995–1002Google Scholar
  157. Suzuki K, Iwamoto K, Yokoyama S, Ikawa T (1991) Glycolate-oxidizing enzymes in algae. J Phycol 27:492–498Google Scholar
  158. Tachibana M, Allen AE, Kikutani S, Endo Y, Bowler C, Matsuda Y (2011) Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth Res 109:205–221PubMedGoogle Scholar
  159. Tanaka Y, Nakatsuma D, Harada H, Ishida M, Matsuda Y (2005) Localization of soluble β-carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Sorting to the chloroplast and cluster formation on the girdle lamellae. Plant Physiol 138:207–217PubMedCentralPubMedGoogle Scholar
  160. Tanaka R, Kikutani S, Mahardika A, Matsuda Y (2014) Localization of enzymes relating to C4 organic acid metabolisms in the marine diatom, Thalassiosira pseudonana. Photosynth Res. doi: 10.1007/s11120-014-9968-9 PubMedGoogle Scholar
  161. Tchernov D, Hassidim M, Luz B, Sukenik A, Reinhold L, Kaplan A (1997) Sustained net CO2 evolution during photosynthesis by marine microorganism. Curr Biol 7:723–728PubMedGoogle Scholar
  162. Teich R, Zauner S, Baurain D, Brinkmann H, Petersen J (2007) Origin and distribution of Calvin cycle fructose and sedoheptulase bisphosphatases in plantae and complex algae: a single secondary origin of complex red plastids and subsequent propagation via tertiary endosymbioses. Protist 158:263–276PubMedGoogle Scholar
  163. Tréguer P, Nelson DM, Bennekom AJ, DeMaster DJ, Leynaert A, Quéquiner B (1995) The silica balance in the world ocean: a reestimate. Science 268:375–379PubMedGoogle Scholar
  164. Trimborn S, Lundholm N, Thomas S, Richter KU, Krock B, Hansen PJ, Rost B (2008) Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: the effect of pH-induced changes in seawater carbonate chemistry. Physiol Plant 133:92–105PubMedGoogle Scholar
  165. Tripp BC, Smith K, Ferry JG (2001) Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276:48615–48618PubMedGoogle Scholar
  166. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737PubMedGoogle Scholar
  167. Van K, Spalding MH (1999) Periplasmic carbonic anhydrase structural gene (Cah1) mutant in Chlamydomonas reinhardtii. Plant Physiol 120:757–764PubMedCentralPubMedGoogle Scholar
  168. Vaughn KC, Campbell EO, Hasegawa J, Owen HA, Renzaglia KS (1990) The pyrenoid is the site of ribulose 1,5-bisphosphate carboxylase/oxygenase accumulation in the hornwort (Bryophyta: Anthocerotae) chloroplast. Protoplasma 156:117–129Google Scholar
  169. Viparelli F, Monti SM, De Simone G, Innocenti A, Scozzafava A, Xu Y, Morel FMM, Supuran CT (2010) Inhibition of the R1 fragment of the cadmium-containing ζ-class carbonic anhydrase from the diatom Thalassiosira weissflogii with anions. Bioorg Med Chem Lett 20:4745–4748PubMedGoogle Scholar
  170. Wang Y, Spalding MH (2006) An inorganic carbon transport system responsible for acclimation specific to air levels of CO2 in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 103:10110–10115PubMedCentralPubMedGoogle Scholar
  171. Wang Y, Sun ZH, Horken KM, Im CS, Xiang Y, Grossman AR, Weeks DP (2005) Analyses of CIA5, the master regulator of the carbon-concentrating mechanism in Chlamydomonas reinhardtii, and its control of gene expression. Can J Bot 83:765–779Google Scholar
  172. Weber T, Gruber A, Kroth PG (2009) The presence and localization of thioredoxins in diatoms, unicellular algae of secondary endosymbiotic origin. Mol Plant 2:468–477PubMedGoogle Scholar
  173. Wilhelm C, Büchel C, Fisahn J, Goss R, Jakob T, Laroch J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124PubMedGoogle Scholar
  174. Wittpoth C, Kroth PG, Weyrauch K, Kowallik KV, Strotmann H (1998) Functional characterization of isolated plastids from two marine diatoms. Planta 206:79–85Google Scholar
  175. Xiang YB, Zhang J, Weeks DP (2001) The Cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 98:5341–5346PubMedCentralPubMedGoogle Scholar
  176. Xu Y, Feng L, Jeffrey PD, Morel FMM (2008) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61PubMedGoogle Scholar
  177. Yamano T, Miura K, Fukuzawa H (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 147:340–354PubMedCentralPubMedGoogle Scholar
  178. Yamano T, Tsujikawa T, Hatano K, Ozawa SI, Takahashi Y, Fukuzawa H (2010) Light and low-CO2 dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol 51:1453–1468PubMedGoogle Scholar
  179. Ynalvez RA, Xiano Y, Ward AS, Cunnusamy K, Moroney JV (2008) Identification and characterization of two closely related β-carbonic anhydrases from Chlamydomonas reinhardtii. Physiol Plant 133:15–26PubMedGoogle Scholar
  180. Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci U S A 99:15507–15512PubMedCentralPubMedGoogle Scholar
  181. Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE (2000) Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 36:379–386Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2014

Authors and Affiliations

  1. 1.Department of Bioscience, Research Center for Environmental BioscienceKwansei Gakuin UniversitySandaJapan
  2. 2.Fachbereich BiologieUniversität KonstanzKonstanzGermany

Personalised recommendations