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The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles

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Abstract

Aquatic photosynthetic organisms, such as the green alga Chlamydomonas reinhardtii, respond to low CO2 conditions by inducing a CO2 concentrating mechanism (CCM). Carbonic anhydrases (CAs) are important components of the CCM. CAs are zinc-containing metalloenzymes that catalyze the reversible interconversion of CO2 and HCO3 . In C. reinhardtii, there are at least 12 genes that encode CA isoforms, including three alpha, six beta, and three gamma or gamma-like CAs. The expression of the three alpha and six beta genes has been measured from cells grown on elevated CO2 (having no active CCM) versus cells growing on low levels of CO2 (with an active CCM) using northern blots, differential hybridization to DNA chips and quantitative RT-PCR. Recent RNA-seq profiles add to our knowledge of the expression of all of the CA genes. In addition, protein content for some of the CA isoforms was estimated using antibodies corresponding to the specific CA isoforms: CAH1/2, CAH3, CAH4/5, CAH6, and CAH7. The intracellular location of each of the CA isoforms was elucidated using immunolocalization and cell fractionation techniques. Combining these results with previous studies using CA mutant strains, we will discuss possible physiological roles of the CA isoforms concentrating on how these CAs might contribute to the acquisition and retention of CO2 in C. reinhardtii.

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References

  • Alber BE, Ferry JG (1994) A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci USA 91:6909–6913

    Article  PubMed  CAS  Google Scholar 

  • Amoroso G, Morell-Avrahov L, Muller D, Klug K, Sultemeyer D (2005) The gene NCE103 (YNL036w) from Saccharomyces cerevisiae encodes a functional carbonic anhydrase and its transcription is regulated by the concentration of inorganic carbon in the medium. Mol Microbiol 56:549–558

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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, Kroger 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 306:79–86

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Price GD (1994) The role of carbonic-anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45:369–392

    Article  CAS  Google Scholar 

  • Badger MR, Kaplan A, Berry JA (1980) Internal inorganic carbon pool of Chlamydomonas-reinhardtii—evidence for a carbon-dioxide concentrating mechanism. Plant Physiol 66:407–413

    Article  PubMed  CAS  Google Scholar 

  • Berry JA, Kaplan A, Badger M (1978) Evidence for a CO2 concentrating mechanism in alga Chlamydomonas reinhardtii. Plant Physiol 61:38–39

    Article  Google Scholar 

  • Borkhsenious ON, Mason CB, Moroney JV (1998) The intracellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. Plant Physiol 116:1585–1591

    Article  PubMed  CAS  Google Scholar 

  • 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, Kroger 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 456:239–244

    Article  PubMed  CAS  Google Scholar 

  • Bracey MH, Christiansen J, Tovar P, Cramer SP, Bartlett SG (1994) Spinach carbonic anhydrase: investigation of the zinc-binding ligands by site-directed mutagenesis, elemental analysis, and Exafs. Biochemistry 33:13126–13131

    Article  PubMed  CAS  Google Scholar 

  • Braun HP, Zabaleta E (2007) Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (Complex I) in plants. Physiol Plant 129:114–122

    Article  CAS  Google Scholar 

  • Burnell JN, Gibbs MJ, Mason JG (1990) Spinach chloroplastic carbonic anhydrase: nucleotide sequence analysis of cDNA. Plant Physiol 92:37–40

    Article  PubMed  CAS  Google Scholar 

  • Cardol P, Vanrobaeys F, Devreese B, Van Beeumen J, Matagne RF, Remacle C (2004) Higher plant-like subunit composition of mitochondrial complex I from Chlamydomonas reinhardtii: 31 conserved components among eukaryotes. Biochim Biophys Acta 1658:212–224

    Article  PubMed  CAS  Google Scholar 

  • Cardol P, Gonzalez-Halphen D, Reyes-Prieto A, Baurain D, Matagne RF, Remacle C (2005) The mitochondrial oxidative phosphorylation proteome of Chlamydomonas reinhardtii deduced from the genome sequencing project. Plant Physiol 137:447–459

    Article  PubMed  CAS  Google Scholar 

  • Chirica LC, Elleby B, Lindskog S (2001) Cloning, expression and some properties of alpha-carbonic anhydrase from Helicobacter pylori. Biochim Biophys Acta 1544:55–63

    Article  PubMed  CAS  Google Scholar 

  • Coleman JR, Grossman AR (1984) Biosynthesis of carbonic-anhydrase in Chlamydomonas reinhardtii during adaptation to low CO2. Proc Natl Acad Sci USA 81:6049–6053

    Article  PubMed  CAS  Google Scholar 

  • Coleman JR, Berry JA, Togasaki RK, Grossman AR (1984) Identification of extracellular carbonic-anhydrase of Chlamydomonas-reinhardtii. Plant Physiol 76:472–477

    Article  PubMed  CAS  Google Scholar 

  • Duanmu D, Wang Y, Spalding MH (2009) Thylakoid lumen carbonic anhydrase (CAH3) mutation suppresses air-Dier phenotype of LCIB mutant in Chlamydomonas reinhardtii. Plant Physiol 149:929–937

    Article  PubMed  CAS  Google Scholar 

  • Elleby B, Chirica LC, Tu C, Zeppezauer M, Lindskog S (2001) Characterization of carbonic anhydrase from Neisseria gonorrhoeae. Eur J Biochem 268:1613–1619

    Article  PubMed  CAS  Google Scholar 

  • Eriksson M, Gardestrom P, Samuelsson G (1995) Isolation, purification, and characterization of mitochondria from Chlamydomonas reinhardtii. Plant Physiol 107:479–483

    PubMed  CAS  Google Scholar 

  • Eriksson M, Karlsson J, Ramazanov Z, Gardestrom P, Samuelsson G (1996) Discovery of an algal mitochondrial carbonic anhydrase: molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 93:12031–12034

    Article  PubMed  CAS  Google Scholar 

  • Eriksson M, Villand P, Gardestrom P, Samuelsson G (1998) Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 116:637–641

    Article  PubMed  CAS  Google Scholar 

  • Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D (2007) Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 30:617–629

    Article  PubMed  CAS  Google Scholar 

  • Fawcett TW, Browse JA, Volokita M, Bartlett SG (1990) Spinach carbonic anhydrase primary structure deduced from the sequence of a cDNA clone. J Biol Chem 265:5414–5417

    PubMed  CAS  Google Scholar 

  • Fujiwara S, Fukuzawa H, Tachiki A, Miyachi S (1990) Structure and differential expression of 2 genes encoding carbonic-anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87:9779–9783

    Article  PubMed  CAS  Google Scholar 

  • Fukuzawa H, Fujiwara S, Tachiki A, Miyachi S (1990a) Nucleotide sequences of two genes CAH1 and CAH2 which encode carbonic anhydrase polypeptides in Chlamydomonas reinhardtii. Nucleic Acids Res 18:6441–6442

    Article  PubMed  CAS  Google Scholar 

  • Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisiosese ML, Miyachi S (1990b) cDNA cloning, sequence, and expression of carbonic-anhydrase in Chlamydomonas reinhardtii—regulation by environmental CO2 concentration. Proc Natl Acad Sci USA 87:4383–4387

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 89:4437–4441

    Article  PubMed  CAS  Google Scholar 

  • Fukuzawa H, Ishizaki K, Miura K, Matsueda S, Ino-ue T, Kucho K, Ohyama K (1998) Isolation and characterization of high-CO2 requiring mutants from Chlamydomonas reinhardtii by gene tagging. Can J Bot 76:1092–1097

    CAS  Google Scholar 

  • Fukuzawa H, Miura K, Ishizaki K, Kucho K, 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 USA 98:5347–5352

    Article  PubMed  CAS  Google Scholar 

  • 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 114:237–244

    Article  PubMed  CAS  Google Scholar 

  • Geraghty AM, Spalding MH (1996) Molecular and structural changes in Chlamydomonas under limiting CO2—a possible mitochondrial role in adaptation. Plant Physiol 111:1339–1347

    PubMed  CAS  Google Scholar 

  • Giordano M, Norici A, Forssen M, Eriksson M, Raven JA (2003) An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132:2126–2134

    Article  PubMed  CAS  Google Scholar 

  • Gotz R, Gnann A, Zimmermann FK (1999) Deletion of the carbonic anhydrase-like gene NCE103 of the yeast Saccharomyces cerevisiae causes an oxygen-sensitive growth defect. Yeast 15:855–864

    Article  PubMed  CAS  Google Scholar 

  • Hanson DT, Franklin LA, Samuelsson G, Badger MR (2003) The Chlamydomonas reinhardtii cia3 mutant lacking a thylakoid lumen-localized carbonic anhydrase is limited by CO2 supply to rubisco and not photosystem II function in vivo. Plant Physiol 132:2267–2275

    Article  PubMed  CAS  Google Scholar 

  • Hewett-Emmett D, Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol 5:50–77

    Article  PubMed  CAS  Google Scholar 

  • Im CS, Zhang ZD, Shrager J, Chang CW, Grossman AR (2003) Analysis of light and CO2 regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosyn Res 75:111–125

    Article  PubMed  CAS  Google Scholar 

  • Ishida S, Muto S, Miyachi S (1993) Structural-analysis of periplasmic carbonic anhydrase-1 of Chlamydomonas reinhardtii. Eur J Biochem 214:9–16

    Article  PubMed  CAS  Google Scholar 

  • Kamo T, Shimogawara K, Fukuzawa H, Muto S, Miyachi S (1990) Subunit constitution of carbonic anhydrase from Chlamydomonas reinhardtii. Eur J Biochem 192:557–562

    Article  PubMed  CAS  Google Scholar 

  • Karlsson J, Hiltonen T, Husic HD, Ramazanov Z, Samuelsson G (1995) Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 109:533–539

    Article  PubMed  CAS  Google Scholar 

  • Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G (1998) A novel alpha-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17:1208–1216

    Article  PubMed  CAS  Google Scholar 

  • Khalifah RG (1971) Carbon dioxide hydration activity of carbonic anhydrase. 1. Stop-flow kinetic studies on native human isoenzyme-B and isoenzyme-C. J Biol Chem 246:2561–2573

    Google Scholar 

  • Kimber MS, Pai EF (2000) The active site architecture of Pisum sativum beta-carbonic anhydrase is a mirror image of that of alpha-carbonic anhydrases. EMBO J 19:1407–1418

    Article  PubMed  CAS  Google Scholar 

  • Kimpel DL, Togasaki RK, Miyachi S (1983) Carbonic-anhydrase in Chlamydomonas reinhardtii I. Localization. Plant Cell Physiol 24:255–259

    CAS  Google Scholar 

  • Klodmann J, Sunderhaus S, Nimtz M, Jansch L, Braun H-P (2010) Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell 22:797–810

    Article  PubMed  CAS  Google Scholar 

  • 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 49:273–283

    Article  PubMed  CAS  Google 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:e1426. doi:10.1371/journal.pone.0001426

  • 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 69:1062–1069

    Article  CAS  Google Scholar 

  • Kucho K, Ohyama K, Fukuzawa H (1999) CO2-responsive transcriptional regulation of cah1 encoding carbonic anhydrase is mediated by enhancer and silencer regions in Chlamydomonas reinhardtii. Plant Physiol 121:1329–1337

    Article  PubMed  CAS  Google Scholar 

  • Kucho K, Yoshioka S, Taniguchi F, Ohyama K, Fukuzawa H (2003) Cis-acting elements and DNA-binding proteins involved in CO2-responsive transcriptional activation of CAH1 encoding a periplasmic carbonic anhydrase Chlamydomonas reinhardtii. Plant Physiol 133:783–793

    Article  PubMed  CAS  Google Scholar 

  • Lane TW, Morel FMM (2000) Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol 123:345–352

    Article  PubMed  CAS  Google Scholar 

  • Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM (2005) A cadmium enzyme from a marine diatom. Nature 435:42–43

    Article  PubMed  CAS  Google Scholar 

  • Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74:1–20

    Google Scholar 

  • Maeda S, Badger MR, Price GD (2002a) Novel gene products associated with NdhD3/D4-containing NDH-1complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol Microbiol 43:425–435

    Article  PubMed  CAS  Google Scholar 

  • Maeda S, Omata T, Badger MR, Price GD (2002b) Mutation of a low-affinity CO2 uptake system leads to a constitutive, high-affinity state for inorganic carbon uptake in the cyanobacterium Synechococcus sp. PCC7942. Plant and Cell Physiol 43:S67–S68

    Google Scholar 

  • McGinn PJ, Morel FMM (2008) Expression and regulation of carbonic anhydrases in the marine diatom Thalassiosira pseudonana and in natural phytoplankton assemblages from great bay, New Jersey. Physiol Plant 133:78–91

    Article  PubMed  CAS  Google Scholar 

  • Meldrum NU, Roughton FJ (1933) Carbonic anhydrase. Its preparation and properties. J Physiol 80:113–142

    PubMed  CAS  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    Article  PubMed  CAS  Google Scholar 

  • Mitra M, Lato SM, Ynalvez RA, Xiao Y, Moroney JV (2004) Identification of a new chloroplast carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 135:173–182

    Article  PubMed  CAS  Google Scholar 

  • Mitra M, Mason CB, Xiao Y, Ynalvez RA, Lato SM, Moroney JV (2005) The carbonic anhydrase gene families of Chlamydomonas reinhardtii. Can J Bot 83:780–795

    Article  CAS  Google Scholar 

  • 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 29:211–219

    Article  CAS  Google Scholar 

  • 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 135:1595–1607

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Tolbert NE (1985) Inorganic carbon uptake by Chlamydomonas reinhardtii. Plant Physiol 77:253–258

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6:1251–1259

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic-anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Tolbert NE, Sears BB (1986) Complementation analysis of the inorganic carbon concentrating mechanism of Chlamydomonas reinhardtii. Mol Gen Genet 204:199–203

    Article  CAS  Google Scholar 

  • Moroney JV, Togasaki RK, Husic HD, Tolbert NE (1987) Evidence that an internal carbonic anhydrase is present in 5% CO2-grown and air-grown Chlamydomonas. Plant Physiol 84:757–761

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Husic HD, Tolbert NE, Kitayama M, Manuel LJ, Togasaki RK (1989) Isolation and characterization of a mutant of Chlamydomonas reinhardtii deficient in the CO2 concentrating mechanism. Plant Physiol 89:897–903

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24:141–153

    Article  CAS  Google Scholar 

  • Newman EA (1994) A physiological measure of carbonic anhydrase in Müller cells. Glia 11:291–299

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  PubMed  CAS  Google Scholar 

  • Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Jancek S, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 104:7705–7710

    Article  PubMed  CAS  Google Scholar 

  • Park YI, Karlsson J, Rojdestvenski I, Pronina N, Klimov V, Oquist G, Samuelsson G (1999) Role of a novel photosystem II-associated carbonic anhydrase in photosynthetic carbon assimilation in Chlamydomonas reinhardtii. FEBS Lett 444:102–105

    Article  PubMed  CAS  Google Scholar 

  • Park H, Song B, Morel FMM (2007) Diversity of the cadmium-containing carbonic anhydrase in marine diatoms and natural waters. Environ Microbiol 9:403–413

    Article  PubMed  CAS  Google Scholar 

  • Peers G, Niyogi KK (2008) Pond scum genomics: the genomes of Chlamydomonas and Ostreococcus. Plant Cell 20:502–507

    Article  PubMed  CAS  Google Scholar 

  • Perales M, Eubel H, Heinemeyer J, Colaneri A, Zabaleta E, Braun HP (2005) Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I + III2 levels and alters mitochondrial physiology in Arabidopsis. J Mol Biol 350:263–277

    Article  PubMed  CAS  Google Scholar 

  • Raven JA (1997) CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ 20:147–154

    Article  CAS  Google Scholar 

  • Raven JA (2001) A role for mitochondrial carbonic anhydrase in limiting CO2 leakage from low CO2-grown cells of Chlamydomonas reinhardtii. Plant Cell Environ 24:261–265

    Article  CAS  Google Scholar 

  • Rawat M, Moroney JV (1991) Partial characterization of a new isoenzyme of carbonic-anhydrase isolated from Chlamydomonas reinhardtii. J Biol Chem 266:9719–9723

    PubMed  CAS  Google Scholar 

  • Rawat M, Henk MC, Lavigne LL, Moroney JV (1996) Chlamydomonas reinhardtii mutants without ribulose-1,5-bisphosphate carboxylase-oxygenase lack a detectable pyrenoid. Planta 198:263–270

    Article  CAS  Google Scholar 

  • Roberts SB, Lane TW, Morel FMM (1997) Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 33:845–850

    Article  CAS  Google Scholar 

  • Rojdestvenski I, Park YI, Karlsson J, Oquist G, Samuelsson G (2000) A carbonic anhydrase catalyzed CO2 pump in Chlamydomonas reinhardtii: in vivo experiments, computer modelling, and theory. Russ J Plant Physiol 47:613–621

    CAS  Google Scholar 

  • Rowlett RS, Chance MR, Wirt MD, Sidelinger DE, Royal JR, Woodroffe M, Wang YF, Saha RP, Lam MG (1994) Kinetic and structural characterization of spinach carbonic anhydrase. Biochem 33:13967–13976

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Shutova T, Kenneweg H, Buchta J, Nikitina J, Terentyev V, Chernyshov S, Andersson B, Allakhverdiev SI, Klimov VV, Dau H, Junge W, Samuelsson G (2008) The photosystem II-associated CAH3 in Chlamydomonas enhances the O2 evolution rate by proton removal. EMBO J 27:782–791

    Article  PubMed  CAS  Google Scholar 

  • Smith KS, Ferry JG (1999) A plant-type (beta-class) carbonic anhydrase in the Thermophilic methanoarchaeon Methanobacterium thermoautotrophicum. J Bacteriol 181:6247–6253

    PubMed  CAS  Google Scholar 

  • So AKC, Espie GS (2005) Cyanobacterial carbonic anhydrases. Can J Bot 83:721–734

    Article  CAS  Google Scholar 

  • So AK, Espie GS, Williams EB, Shively JM, Heinhorst S, Cannon GC (2004) A novel evolutionary lineage of carbonic anhydrase (epsilon class) is a component of the carboxysome shell. J Bacteriol 186:623–630

    Article  PubMed  CAS  Google Scholar 

  • Soltes-Rak E, Mulligan ME, Coleman JR (1997) Identification and characterization of a gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria. J Bacteriol 179:769–774

    PubMed  CAS  Google Scholar 

  • Spalding MH, Spreitzer RJ, Ogren WL (1983) Carbonic anhydrase-deficient mutant of Chlamydomonas reinhardii requires elevated carbon-dioxide concentration for photoautotrophic growth. Plant Physiol 73:268–272

    Article  PubMed  CAS  Google Scholar 

  • Spencer KG, Kimpel DL, Fisher ML, Togasaki RK, Miyachi S (1983) Carbonic-anhydrase in Chlamydomonas reinhardtii II. Requirements for carbonic-anhydrase induction. Plant Cell Physiol 24:301–304

    CAS  Google Scholar 

  • Sunderhaus S, Dudkina NV, Jansch L, Klodmann J, Heinemeyer J, Perales M, Zabaleta E, Boekema EJ, Braun HP (2006) Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants. J Biol Chem 281:6482–6488

    Article  PubMed  CAS  Google Scholar 

  • Tachiki A, Fukuzawa H, Miyachi S (1992) Characterization of carbonic-anhydrase isozyme CA2, which is the CAH2 gene-product, in Chlamydomonas reinhardtii. Biosci Biotechnol Biochem 56:794–798

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) Mega4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S, Cannon GC, Yeates TO (2008) Atomic-level models of the bacterial carboxysome shell. Science 319:1083–1086

    Article  PubMed  CAS  Google Scholar 

  • Tsuzuki M, Miyachi S (1979) Effects of CO2 concentration during growth and of ethoxyzolamide on CO2 compensation point in chlorella. FEBS Lett 103:221–223

    Article  PubMed  CAS  Google Scholar 

  • Tsuzuki M, Miyachi S (1989) The function of carbonic-anhydrase in aquatic photosynthesis. Aquat Bot 34:85–104

    Article  CAS  Google Scholar 

  • Tsuzuki M, Shiraiwa Y, Miyachi S (1980) Role of carbonic-anhydrase in photosynthesis in Chlorella derived from kinetic-analysis of 14CO2 fixation. Plant Cell Physiol 21:677–688

    CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Van K, Spalding MH (1999) Periplasmic carbonic anhydrase structural gene (cah1) mutant in Chlamydomonas reinhardtii. Plant Physiol 120:757–764

    Article  PubMed  CAS  Google Scholar 

  • Villand P, Eriksson M, Samuelsson G (1997) Carbon dioxide and light regulation of promoters controlling the expression of mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Biochem J 327:51–57

    PubMed  CAS  Google Scholar 

  • Villarejo A, Shutova T, Moskvin O, Forssen M, Klimov VV, Samuelsson G (2002) A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution. EMBO J 21:1930–1938

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 103:10110–10115

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Spalding MH (2007) LCIB functions in a multi-subunit complex essential for inorganic carbon transport in Chlamydomonas reinhardtii. Photosyn Res 91:221–222

    Google Scholar 

  • Wang Y, Sun ZH, Horken KM, Im CS, Xiang YB, 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 83:765–779

    Article  CAS  Google Scholar 

  • Xiang YB, Zhang J, Weeks DP (2001) The CIA5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 98:5341–5346

    Article  PubMed  CAS  Google Scholar 

  • Yamano T, Fukuzawa H (2009) Carbon-concentrating mechanism in a green alga, Chlamydomonas reinhardtii, revealed by transcriptome analyses. J Basic Microbiol 49:42–51

    Article  PubMed  CAS  Google Scholar 

  • 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 147:340–354

    Article  PubMed  CAS  Google Scholar 

  • 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 51:1453–1468

    Article  PubMed  CAS  Google Scholar 

  • Ynalvez RA, Xiao Y, Ward AS, Cunnusamy K, Moroney JV (2008) Identification and characterization of two closely related beta-carbonic anhydrases from Chlamydomonas reinhardtii. Physiol Plant 133:15–26

    Article  PubMed  CAS  Google Scholar 

  • Yoshioka S, Taniguchi F, Miura K, Inoue T, Yamano T, Fukuzawa H (2004) The novel Myb transcription factor LCR1 regulates the CO2-responsive gene CAH1, encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Cell 16:1466–1477

    Article  PubMed  CAS  Google Scholar 

  • Yu JW, Price GD, Song L, Badger MR (1992) Isolation of a putative carboxysomal carbonic-anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100:794–800

    Article  PubMed  CAS  Google Scholar 

  • Yuan Q, Ouyang S, Wang A, Zhu W, Maiti R, Lin H, Hamilton J, Haas B, Sultana R, Cheung F, Wortman J, Buell CR (2005) The institute for genomic research Osa1 rice genome annotation database. Plant Physiol 138:18–19

    Article  PubMed  CAS  Google Scholar 

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Moroney, J.V., Ma, Y., Frey, W.D. et al. The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 109, 133–149 (2011). https://doi.org/10.1007/s11120-011-9635-3

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