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.
Similar content being viewed by others
References
Alber BE, Ferry JG (1994) A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci USA 91:6909–6913
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
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
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
Badger MR, Price GD (1994) The role of carbonic-anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45:369–392
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
Berry JA, Kaplan A, Badger M (1978) Evidence for a CO2 concentrating mechanism in alga Chlamydomonas reinhardtii. Plant Physiol 61:38–39
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
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
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
Braun HP, Zabaleta E (2007) Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (Complex I) in plants. Physiol Plant 129:114–122
Burnell JN, Gibbs MJ, Mason JG (1990) Spinach chloroplastic carbonic anhydrase: nucleotide sequence analysis of cDNA. Plant Physiol 92:37–40
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
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
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
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
Coleman JR, Berry JA, Togasaki RK, Grossman AR (1984) Identification of extracellular carbonic-anhydrase of Chlamydomonas-reinhardtii. Plant Physiol 76:472–477
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
Elleby B, Chirica LC, Tu C, Zeppezauer M, Lindskog S (2001) Characterization of carbonic anhydrase from Neisseria gonorrhoeae. Eur J Biochem 268:1613–1619
Eriksson M, Gardestrom P, Samuelsson G (1995) Isolation, purification, and characterization of mitochondria from Chlamydomonas reinhardtii. Plant Physiol 107:479–483
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Ishida S, Muto S, Miyachi S (1993) Structural-analysis of periplasmic carbonic anhydrase-1 of Chlamydomonas reinhardtii. Eur J Biochem 214:9–16
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
Karlsson J, Hiltonen T, Husic HD, Ramazanov Z, Samuelsson G (1995) Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 109:533–539
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
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
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
Kimpel DL, Togasaki RK, Miyachi S (1983) Carbonic-anhydrase in Chlamydomonas reinhardtii I. Localization. Plant Cell Physiol 24:255–259
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
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
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
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
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
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
Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM (2005) A cadmium enzyme from a marine diatom. Nature 435:42–43
Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74:1–20
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
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
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
Meldrum NU, Roughton FJ (1933) Carbonic anhydrase. Its preparation and properties. J Physiol 80:113–142
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
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
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
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
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
Moroney JV, Tolbert NE (1985) Inorganic carbon uptake by Chlamydomonas reinhardtii. Plant Physiol 77:253–258
Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6:1251–1259
Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic-anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183
Moroney JV, Tolbert NE, Sears BB (1986) Complementation analysis of the inorganic carbon concentrating mechanism of Chlamydomonas reinhardtii. Mol Gen Genet 204:199–203
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
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
Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24:141–153
Newman EA (1994) A physiological measure of carbonic anhydrase in Müller cells. Glia 11:291–299
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
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
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
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
Peers G, Niyogi KK (2008) Pond scum genomics: the genomes of Chlamydomonas and Ostreococcus. Plant Cell 20:502–507
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
Raven JA (1997) CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ 20:147–154
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
Rawat M, Moroney JV (1991) Partial characterization of a new isoenzyme of carbonic-anhydrase isolated from Chlamydomonas reinhardtii. J Biol Chem 266:9719–9723
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
Roberts SB, Lane TW, Morel FMM (1997) Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 33:845–850
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
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
Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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
Smith KS, Ferry JG (1999) A plant-type (beta-class) carbonic anhydrase in the Thermophilic methanoarchaeon Methanobacterium thermoautotrophicum. J Bacteriol 181:6247–6253
So AKC, Espie GS (2005) Cyanobacterial carbonic anhydrases. Can J Bot 83:721–734
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
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
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
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
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
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
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
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
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
Tsuzuki M, Miyachi S (1989) The function of carbonic-anhydrase in aquatic photosynthesis. Aquat Bot 34:85–104
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
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
Van K, Spalding MH (1999) Periplasmic carbonic anhydrase structural gene (cah1) mutant in Chlamydomonas reinhardtii. Plant Physiol 120:757–764
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
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
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
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
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
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
Yamano T, Fukuzawa H (2009) Carbon-concentrating mechanism in a green alga, Chlamydomonas reinhardtii, revealed by transcriptome analyses. J Basic Microbiol 49:42–51
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
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
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
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
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
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
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-011-9635-3