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The Uptake of CO2 by Cyanobacteria and Microalgae

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Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 34))

Summary

Cyanobacteria and eukaryotic algae possess a CO2-concentrating mechanism (CCM), which involves the transport of inorganic carbon (Ci) driven by light energy and the fixation of CO2 in the subcellular compartments (carboxysomes in cyanobacteria and pyrenoids in green algae) where most of the ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) is confined. Physiological and molecular analysis identified five Ci uptake-systems in cyanobacteria. Two of them are CO2-uptake systems driven by the thylakoid membrane-located NAD(P)H dehydrogenase (NDH-1) complexes. Three bicarbonate transporters, BCT1 (an ABC-type transporter composed of Cmp proteins), SbtA and BicA, are localized on the cytoplasmic membranes. One of the main features of the CCMs is a marked rise in the ability to take up Ci observed when high-CO2-grown cells are transferred to CO2-limiting conditions in the light. Many low-CO2 (LC)-inducible genes including those involved in Ci uptake have been identified in cyanobacteria and green algae. Chlamydomonas reinhardtii is a model eukaryotic alga and has been used extensively for the study of the CCM. Candidate genes responsible for Ci uptake in C. reinhardtii, and that encode proteins homologous to transporters in other organisms, were found among LC-inducible genes identified by DNA microarray analysis. These genes include LciA and LciB, whose transcripts are not accumulated in the pmp1 mutant defective in Ci-transport upon exposure to LC. The CCM1 (CIA5) is essential for the control of CCM induction and the expression of CO2-responsive genes through putative LC signal transduction pathways. We present recent studies on the mechanisms of CO2-sensing and of induction of gene expression by LC. Other microalgae such as coccolithophorids, diatoms and dinoflagellates also possess CCMs. We summarize the present state of the art on the CCMs of these major aquatic primary producers and other CCM-related topics such as cycling of Ci, CO2-mediated interspecies communication, stable carbon isotope fractionation and biotechnological implications.

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Abbreviations

CA –:

Carbonic anhydrase;

CCM –:

CO2-Concentrating mechanism;

Ci – :

Inorganic carbon;

HC –:

High CO2;

HCR –:

High-CO2-requring;

LC –:

Low CO2;

NDH-1 –:

NAD(P)H dehydrogenase;

PS –:

Photosystem;

Rubisco –:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, 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 WWY, 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 and 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 and Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54: 609–622

    Article  PubMed  CAS  Google Scholar 

  • Badger MR and Spalding MH (2000) CO2 acquisition, concentration and fixation in cyanobacteria and algae. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, Advances in Photosynthesis, Vol 9, pp 369–397. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Badger MR, Kaplan A, and 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 

  • Badger MR, Palmqvist K and Yu JW (1994) Measurement of CO2 and HCO −3 fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol Plant 90: 529–536

    Article  CAS  Google Scholar 

  • Badger MR, Price GD, Long BM and Woodger FJ (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57: 249–265

    Article  PubMed  CAS  Google Scholar 

  • Ball SG (1998) Regulation of starch biosynthesis. In: Rochaix JD, Goldschmidt-Clermont M and Merchant S (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, Advances in Photosynthesis, Vol 7, pp 549–567. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Battchikova N and Aro EM (2007) Cyanobacterial NDH-1 complexes: multiplicity in function and subunit composition. Physiol Plant 131: 22–32

    Article  PubMed  CAS  Google Scholar 

  • Battchikova N, Zhang PP, Rudd S, Ogawa T and Aro EM (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L, and NDH-1M complexes of Synechocystis sp. PCC 6803. J Biol Chem 280: 2587–2595

    Article  PubMed  CAS  Google Scholar 

  • Beardall J and Raven JA (2004) The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43: 26–40

    Article  Google Scholar 

  • Behrenfeld MJ, Bale AJ, Kolber ZS, Aiken J and Falkowski PG (1996) Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383: 508–511

    Article  CAS  Google Scholar 

  • Benthien A, Zondervan I, Engel A, Hefter J, Terbruggen A and Riebesell U (2007) Carbon isotopic fractionation during a mesocosm bloom experiment dominated by Emiliania huxleyi: Effects of CO2 concentration and primary production. Geochim Cosmochim Acta 71: 1528–1541

    Article  CAS  Google Scholar 

  • Berman-Frank I, Erez J and Kaplan A (1998) Changes in inorganic carbon uptake during the progression of dinoflagellate bloom in a lake ecosystem. Can J Bot 76: 1043–1051

    CAS  Google Scholar 

  • Berman-Frank I, Kaplan A, Zohary T and Dubinsky Z (1995) Carbonic anhydrase activity in the bloom-forming dinoflagellate Peridinium gatunense. J Phycol 31: 906–913

    Article  CAS  Google Scholar 

  • Bonfil DJ, Ronen-Tarazi M, Sültemeyer D, Lieman-Hurwitz J, Schatz D and Kaplan A (1998) A putative HCO −3 transporter in the cyanobacterium Synechococcus sp. strain PCC 7942. FEBS Lett 430: 236–240

    Article  PubMed  CAS  Google Scholar 

  • Bowes G, Rao SK, Estavillo GM and Reiskind JB (2004) C4 mechanism in aquatic angiosperms: Comparisons with terrestrial C4 systems. Funct Plant Biol 29: 379–392

    Article  Google Scholar 

  • Bowler C, Allen EA, 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 J-P, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N. Kroth PG, La Roche J, Lindquist E, Lommer M, Marten-Jèzèquel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq M-P, Napoli C, Obornik M, Parker MS, Petit J-L, 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 and Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239–244

    Google Scholar 

  • Bryant DR (ed) (1994) The Molecular Biology of Cyanobacteria, Advances in Photosynthesis, Vol 1, Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Burkhardt S, Amoroso G, Riebesell U and Sültemeyer D (2001) CO2 and HCO −3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46: 1378–1391

    Article  CAS  Google Scholar 

  • Burow MD, Chen ZY, Mouton TM and Moroney JV (1996) Isolation of cDNA clones of genes induced upon transfer of Chlamydomonas reinhardtii cells to low CO2. Plant Mol Biol 31: 443–448

    Article  PubMed  CAS  Google Scholar 

  • Cassar N, Laws EA, Bidigare RR and Popp BN (2004) Bicarbonate uptake by Southern Ocean phytoplankton. Global Biogeochem Cycles 18 Article Number: GB2003

    Google Scholar 

  • Chen XW and Gao KS (2004) Photosynthetic utilisation of inorganic carbon and its regulation in the marine diatom Skeletonema costatum. Funct Plant Biol 31: 1027–1033

    Article  CAS  Google Scholar 

  • Chen ZY, Burow MD, Mason CB and Moroney JV (1996) A low-CO2-inducible gene Encoding an alanine:[alpha]-ketoglutarate aminotransferase in Chlamydomonas reinhardtii. Plant Physiol 112: 677–684

    Article  PubMed  CAS  Google Scholar 

  • Chen ZY, Lavigne LL, Mason CB and Moroney JV (1997) Cloning and overexpression of two cDNAs encoding the low-CO2-inducible chloroplast envelope protein LIP-36 from Chlamydomonas reinhardtii. Plant Physiol 114: 265–273

    Article  PubMed  CAS  Google Scholar 

  • Colman B, Huertas IE, Bhatti S and Dason JS (2002) The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct Plant Biol 29: 261–270

    Article  CAS  Google Scholar 

  • Coleman JR (1991) The molecular and biochemical analyses of CO2 concentrating mechanisms in cyanobacteria and microalgae. Plant Cell Environ 14: 861–867

    Article  CAS  Google Scholar 

  • Dason JS, Huertas IE and Colman B (2004) Source of inorganic carbon for photosynthesis in two marine dinoflagellates. J Phycol 40: 285–292

    Article  CAS  Google Scholar 

  • Duanmu D, Miller AR, Horken KM, Weeks DP and Spalding MH (2009a) Knockdown of limiting-CO2-induced gene HLA3 decreases HCO3– transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 106: 5990–5995

    Google Scholar 

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

    Google Scholar 

  • Edwards GE, Franceschi VR and Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu Rev Plant Biol 55: 173–196

    Article  PubMed  CAS  Google Scholar 

  • 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 phosphoglycolate metabolism in cyanobacteria. Plant Physiol 142: 333–342

    Article  PubMed  CAS  Google Scholar 

  • Eisenhut M, Ruth W, Haimovich M, Bauwe H and Kaplan A (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiotically to plants. Proc Natl Acad Sci USA 105: 17199–17204

    Google Scholar 

  • Engel A, Schulz KG, Riebesell U, Bellerby R, Delille B and Schartau M (2008) Effects of CO2 on particle size distribution and phytoplankton abundance during a mesocosm bloom experiment (PeECE II). Biogeosciences 5: 509–521

    Article  CAS  Google Scholar 

  • Engel A, Zondervan I, Aerts K, Beaufort L, Benthien A, Chou L, Delille B, Gattuso JP, Harlay J, Heemann C, Hoffmann L, Jacquet S, Nejstgaard J, Pizay MD, Rochelle-Newall E, Schneider U, Terbrueggen A and Rebesell U (2005) Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol Oceanogr 50: 493–507

    Article  CAS  Google Scholar 

  • Erez J, Bouevich A and Kaplan A (1998) Carbon isotope fractionation by the freshwater cyanobacterium Synechococcus PCC 7942. Can J Bot 76: 1109–1118

    CAS  Google Scholar 

  • Eriksson M, Karlsson J, Ramazanov Z, Gardestroem P and 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 

  • Espie GS and Colman B (1986) Inorganic carbon uptake during photosynthesis. I: a theoretical analysis using the isotopic disequilibrium technique. Plant Physiol 80: 863–869

    Article  PubMed  CAS  Google Scholar 

  • Espie GS and Kandasamy RA (1994) Monensin inhibition of Na+-dependent HCO −3 transport distinguishes it from Na+-independent HCO −3 transport and provides evidence for Na+/HCO −3 symport in the cyanobacterium Synechococcus UTEX 625. Plant Physiol 104: 1419–1428

    PubMed  CAS  Google Scholar 

  • Espie GS, Miller AG and Canvin DT (1989) Selective and reversible inhibition of active CO2 transport by hydrogen sulfide in a cyanobacterium. Plant Physiol 91: 389–394

    Article  Google Scholar 

  • Falkowski PG (1994) The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth Res 39: 235–258

    Article  CAS  Google Scholar 

  • Falkowski PG and Raven J (1997) Aquatic Photosynthesis. Blackwell Scientific, Oxford

    Google Scholar 

  • Falkowski PG, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hogberg P, Linder S, Mackenzie FT, Moore B, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V and Steffen W (2000) The global carbon cycle: A test of our knowledge of earth as a system. Science 290: 291–296

    Article  PubMed  CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR and Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 503–537

    Article  CAS  Google Scholar 

  • Figge RM, Cassier-Chauvat C, Chauvat F and Cerff R (2001) Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. Mol Microbiol 39: 455–468

    Article  PubMed  CAS  Google Scholar 

  • Folea M, Zhang P, Nowaczyk MM, Ogawa T, Aro E-M and Boekema EJ (2008) Single particle analysis of thylakoid proteins from Thermosynechococcus elongatus and Synechocystis 6803: Localization of the CupA subunit of NDH-1. FEBS Lett 582: 249–254

    Article  PubMed  CAS  Google Scholar 

  • Fukuzawa H, Fujiwara S, Yamamoto Y, Dionizio-Sese ML and Miyachi S (1990) 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, Miura K, Ishizaki K, Kucho K, Saito T, Kohinata T and 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 

  • Fukuzawa H, Suzuki E, Komukai Y and Miyachi S (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC 7942. Proc Natl Acad Sci USA 89: 4437–4441

    Article  PubMed  CAS  Google Scholar 

  • Furla P, Galgani I, Durand I and Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203: 3445–3457

    PubMed  CAS  Google Scholar 

  • Gervais F and Riebesell U (2001) Effect of phosphorus limitation on elemental composition and stable carbon isotope fractionation in a marine diatom growing under different CO2 concentrations. Limnol Oceanogr 46: 497–504

    Article  CAS  Google Scholar 

  • Gervais F, Riebesell U and Gorbunov MY (2002) Changes in primary productivity and chlorophyll a in response to iron fertilization in the Southern Polar Frontal Zone. Limnol Oceanogr 47: 1324–1335

    Article  CAS  Google Scholar 

  • Giordano M, Beardall J and Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Ann Rev Plant Biol 56: 99–131

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Goericke R and Fry B (1994) Variation of marine plankton delta 13C with latitude, temperature, and dissolved CO2 in the world ocean. Global Biochem Cycles 8: 85–90

    Article  CAS  Google Scholar 

  • Guy RD, Fogel ML and Berry JA (1993) Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol 101: 37–47

    PubMed  CAS  Google Scholar 

  • Harada H, Nakatsuma D, Ishida M and 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: 1041–1050

    Article  PubMed  CAS  Google Scholar 

  • Hassidim M, Keren N, Ohad I, Reinhold L and Kaplan A (1997) Acclimation of Synechococcus strain WH7803 to ambient CO2 concentration and to elevated light intensity. J Phycol 33: 811–817

    Article  Google Scholar 

  • Hatch MD (1992) C4 photosynthesis: An unlikely process full of surprises. Plant Cell Physiol 33: 333–342

    CAS  Google Scholar 

  • Herranen M, Battchikova N, Zhang PP, Graf A, Sirpio S, Paakkarinen V and Aro EM (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol 134: 470–481

    Article  PubMed  CAS  Google Scholar 

  • Huertas IE, Espie GS, Colman B and Lubian LM (2000) Light-dependent bicarbonate uptake and CO2 efflux in the marine microalga Nannochloropsis gaditana. Planta 211: 43–49

    Article  PubMed  CAS  Google Scholar 

  • Iglesias-Rodriguez MD, Halloran PR, Rickaby RE, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DR, Tyrrell T, Gibbs SJ, von Dassow P, Rehm E, Armbrust EV and Boessenkool KP (2008) Phytoplankton calcification in a high-CO2 world. Science 320: 336–340

    Article  PubMed  CAS  Google Scholar 

  • Im CS and Grossman AR (2002) Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. Plant J 30: 301–313

    Google Scholar 

  • Jenks A and 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 Peridinium foliaceum (Dinophyceae). J Phycol 36: 127–138

    Article  CAS  Google Scholar 

  • Johnston AM (1991) The acquisition of inorganic carbon by marine macroalgae. Can J Bot 69: 1123–1132

    Article  CAS  Google Scholar 

  • Johnston AM, Maberly SC and Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae from different habitats. Oecologia 91: 481–492

    Article  Google Scholar 

  • Jordan DB and Ogren WL (1981) Species variation in the specificity of ribulose-bisphosphate carboxylase-oxygenase. Nature 291: 513–515

    Article  CAS  Google Scholar 

  • Kaplan A and Reinhold L (1999) The CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539–570

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Hagemann M, Bauwe H, Kahlon S and Ogawa T (2008) Carbon acquisition by cyanobacteria: Mechanisms, comparative genomics, and evolution. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution, pp 305–334. Horizon Scientific Press, Norwich, UK

    Google Scholar 

  • Kaplan A, Marcus Y and Reinhold L (1988) Inorganic carbon uptake by cyanobacteria. In: Packer L and Glazer AN (eds) Methods in Enzymology, Vol 167, pp 534–539. Academic Press, New York

    Google Scholar 

  • Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV and 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 

  • Kim JM, Lee K, Shin K, Kang JH, Lee HW, Kim M, Jang PG and Jang MC (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnol Oceanogr 51: 1629–1636

    Article  CAS  Google Scholar 

  • Kohinata T, Nishino H and 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 

  • Koropatkin NM, Koppenaal DW, Pakrasi HB and Smith TJ (2007) The structure of a cyanobacterial bicarbonate transport protein, CmpA. J Biol Chem 282: 2606–2614

    Article  CAS  Google Scholar 

  • Koumandou VL, Nisbet RER, Barbrook AC and Howe CJ (2004) Dinoflagellate chloroplasts - where have all the genes gone? Trends Genet 20: 261–267

    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 and Bowler C (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3: e1426.

    Article  PubMed  CAS  Google Scholar 

  • Kucho K, Ohyama K and 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 and Fukuzawa H (2003) Cis-acting elements and DNA-binding proteins involved in CO2-responsive transcriptional activation of Cah1 encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 133: 783–793

    Article  PubMed  CAS  Google Scholar 

  • Lane TW and Morell 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 

  • Larsen JB, Larsen A, Thyrhaug R, Bratbak G, and Sandaa RA (2008) Response of marine viral populations to a nutrient induced phytoplankton bloom at different pCO2 levels. Biogeosciences 5: 523–533

    Article  Google Scholar 

  • Laws EA, Popp BN, Cassar N and Tanimoto J (2002) 13C discrimination patterns in oceanic phytoplankton: likely influence of CO2 concentrating mechanisms, and implications for palaeoreconstructions. Funct Plant Biol 29: 323–333

    Article  CAS  Google Scholar 

  • Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, Badger MR and Yellowlees D (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29: 309–322

    Article  CAS  Google Scholar 

  • Li Q and Canvin DT (1998) Energy sources for HCO −3 and CO2 transport in air-grown cells of Synechococcus UTEX 625. Plant Physiol 116: 1125–1132

    Article  PubMed  CAS  Google Scholar 

  • Lieman-Hurwitz J, Haimovich M, Shalev-Maul G, Ishii A, Hihara Y, Gaathon A, Lebendiker M and Kaplan A (2009) A cyanobacterial Abr-B like protein affects the apparent photosynthetic affinity to CO2 by modulating low-CO2-gene expression. Environ Microbiol 11: 927–936

    Google Scholar 

  • Lieman-Hurwitz J, Rachmilevitch S, Mittler RYM and Kaplan A (2003) Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO −3 accumulation in cyanobacteria. Plant Biotech J 1: 43–50

    Article  CAS  Google Scholar 

  • Maberly SS (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26: 439–449

    Article  CAS  Google Scholar 

  • Mackenzie TD, Burns RA and Campbell DA (2004) Carbon status constrains light acclimation in the cyanobacterium Synechococcus elongatus. Plant Physiol 136: 3301–3312

    Article  PubMed  CAS  Google Scholar 

  • McGinn PJ, Price GD, Maleszka R and Badger MR (2003) Inorganic carbon limitation and light control the expression of transcripts related to the CO2-concentrating mechanism in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 132: 218–229

    Article  PubMed  CAS  Google Scholar 

  • Maeda S, Badger MR and 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. PCC 7942. Mol Microbiol 43: 425–436

    Article  PubMed  CAS  Google Scholar 

  • Maeda S, Price GD, Badger MR, Enomoto C and Omata T (2000) Bicarbonate binding activity of the CmpA protein of the cyanobacterium Synechococcus sp. strain PCC 7942 involved in active transport of bicarbonate. J Biol Chem 275: 20551–20555

    Article  PubMed  CAS  Google Scholar 

  • Mamedov TG, Suzuki K, Miura K, Kucho K and Fukuzawa H (2001) Characteristics and sequence of phosphoglycerate phosphatase from an eukaryotic green algae Chlamydomonas reinhardtii. J Biol Chem 276: 45573–45579

    Article  PubMed  CAS  Google Scholar 

  • Marco E, Ohad N, Schwarz R, Lieman-Hurwitz J, Gabay C and Kaplan A (1993) High CO2 concentration alleviates the block in photosynthetic electron transport in an ndhB-inactivated mutant of Synechococcus sp. PCC 7942. Plant Physiol 101: 1047–1053

    Article  PubMed  CAS  Google Scholar 

  • Marcus Y, Schwarz R, Friedberg D and Kaplan A (1986) High CO2 requiring mutant of Anacystis nidulans R2. Plant Physiol 82: 610–612

    Article  PubMed  CAS  Google Scholar 

  • Mariscal V, Moulin P, Orsel M, Miller AJ, Fernández E and Galván A (2006) Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. Protist 157: 421–433

    Article  PubMed  CAS  Google Scholar 

  • Matsuda Y and Colman B (1995) Induction of CO2 and bicarbonate transport in the green Alga Chlorella ellipsoidea. II. Evidence for induction in response to external CO2 concentration. Plant Physiol 108: 253–260

    PubMed  CAS  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250

    Article  PubMed  CAS  Google Scholar 

  • Mi H, Endo T, Ogawa T and Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediated cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36: 661–668

    CAS  Google Scholar 

  • Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1992) Electron donation from cyclic and respiratory flows to photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33: 1233–1237

    CAS  Google Scholar 

  • Miller AG, Espie GS and Canvin DT (1990) Physiological aspects of CO2 and HCO −3 transport by cyanobacteria: a review. Can J Bot 68: 1291–1302

    Article  CAS  Google Scholar 

  • Miller AG, Espie GE and Canvin DT (1991) The use of COS, a structural analog of CO2, to study CO2 transport in the cyanobacterium Synechococcus UTEX 625. Plant Physiol 90: 1221–1231

    Article  Google Scholar 

  • Miller AG, Turpin DH and Canvin DT (1984) Na+ requirement for growth, photosynthesis, and pH regulation in the alkalotolerant cyanobacterium Synechococcus leopoliensis. J Bacteriol 159: 100–106

    PubMed  CAS  Google Scholar 

  • Mitchell C and Beardall J (1996) Inorganic carbon uptake by an Antarctic sea-ice diatom, Nitzschia frigida. Polar Biol 16: 95–99

    Article  Google Scholar 

  • Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT, Ohyama K and 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 

  • Montsant A, Jabbari K, Maheswari U and Bowler C (2005) Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Physiol 137: 500–513

    Article  PubMed  Google Scholar 

  • Morita E, Abe T, Tsuzuki M, Fujiwana S, Sato N, Hirata A, Sonoike K and Nozaki H (2000) Role of pyrenoids in the CO2-concentrating mechanism: comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas. Planta 208: 365–372

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Morse D, Salois P, Markovic P and Hastings JW (1995) A nuclear-encoded form II RuBisCo in dinoflagellates. Science 268: 1622–1624

    Article  PubMed  CAS  Google Scholar 

  • Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP and Allemand D (2005) Stable isotopes (delta C-13 and delta N-15) of organic matrix from coral skeleton. Proc Natl Acad Sci USA 102: 1525–1530

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y, Kanakagiri S, Van, K, He W and Spalding MH (2005) Disruption of glycolate dehydrogenase gene in the high CO2 requiring mutant HCR89 of Chlamydomonas reinhardtii. Can J Bot 83: 820–833

    Article  CAS  Google Scholar 

  • Nassoury N, Fritz L and Morse D (2001) Circadian changes in ribulose-1,5-bisphosphate carboxylase/oxygenase distribution inside individual chloroplasts can account for the rhythm in dinoflagellate carbon fixation. Plant Cell 13: 923–934

    PubMed  CAS  Google Scholar 

  • Nimer N-A, Ling MX, Brownlee C and Merret MJ (1999) Inorganic carbon limitation, exofacial carbonic anhydrase activity, and plasma membrane redox activity in marine phytoplankton species. J Phycol 35: 1200–1205

    Article  CAS  Google Scholar 

  • Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda S and 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. 68:98–109

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T (1990) Mutants of Synechocystis PCC 6803 defective in inorganic carbon transport. Plant Physiol 94: 760–765

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T (1991a) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC 6803. Proc Natl Acad Sci USA 88: 4275–4279

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T (1991b) Cloning and inactivation of a gene essential to inorganic carbon transport of Synechocystis PCC 6803. Plant Physiol 96: 280–284

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T (1992) Identification and characterization of the ictA/ndhL gene product essential to inorganic carbon transport of Synechocystis PCC 6803. Plant Physiol 99: 1604–1608

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T (1993) Molecular analysis of the CO2 concentrating mechanism in cyanobacteria. In: Yamamoto HY and Smith C (eds) Photosynthetic Responses to the Environment, pp 113–125. American Society of Plant Physiologist, Rockville

    Google Scholar 

  • Ogawa T and Kaplan A (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77: 105–115

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T and Mi H (2007) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93:69–77

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T and Ogren WL (1985) Action spectra for accumulation of inorganic carbon in the cyanobacterium, Anabaena variabilis. Photochem Photobiol 41: 583–587

    Article  CAS  Google Scholar 

  • Ogawa T, Miyano A and Inoue Y (1985) Photosystem-I driven inorganic carbon transport in the cyanobacterium, Anacystis nidulans. Biochim Biophys Acta 808: 77–84

    Article  CAS  Google Scholar 

  • Ohkawa H, Pakrasi HB and Ogawa T (2000) Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC6803. J Biol Chem 275: 31630–31634

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Sonoda M, Katoh H and Ogawa T (1998) The use of mutants in the analysis of the CCM in cyanobacteria. Can J Bot 76: 1025–1034

    Google Scholar 

  • Ohkawa H, Sonoda M, Shibata M and Ogawa T (2001) Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. J Bacteriol 183: 4938–4939

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi N, Mukherjee B, Tsujikawa T, Yanase M, Nakano H, Moroney JV and Fukuzawa H (2010) Expression of a low CO2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22: 3105–3117

    Google Scholar 

  • Omata T (1992) Characterization of the downstream region of cmpA: Identification of a gene cluster encoding a putative permease of the cyanobacterium Synechococcus PCC7942. In: Murata N (ed) Research in Photosynthesis, pp. 807–810. Kluwer Academic Publishers, Dordrecht

    Chapter  Google Scholar 

  • Omata T and Ogawa T (1985) Changes in the polypeptide composition of the cytoplasmic membrane of the cyanobacterium Anacystis nidulans during adaptation to low CO2 conditions. Plant Cell Physiol 26: 1075–1081

    CAS  Google Scholar 

  • Omata T and Ogawa T (1986) Biosynthesis of a 42-kD polypeptide in the cytoplasmic membrane of the cyanobacterium Anacystis nidulans strain R2 during adaptation to low CO2 conditions. Plant Physiol 80: 525–530

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Carlson TJ, Ogawa T and Piece J (1990) Sequencing and modification of the gene encoding the 42-kilodalton protein in the cytoplasmic membrane of Synechococcus PCC 7942. Plant Physiol 93: 305–311

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Gohta S, Takahashi Y, Harano Y and Maeda S (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183: 1891–1898

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Price GD, Badger MR, Okamura M, Gohta S and Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. Strain. Proc Natl Acad Sci USA 96: 13571–13576

    Article  PubMed  CAS  Google Scholar 

  • Paasche E (2001) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40: 503–529

    Article  Google Scholar 

  • Pollock SV, Prout DL, Godfrey AC, Lemaire SD and Moroney JV (2004) The Chlamydomonas reinhardtii proteins Ccp1 and Ccp2 are required for long-term growth, but are not necessary for efficient photosynthesis, in a low-CO2 environment. Plant Mol Biol 56: 125–132

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Badger MR, Woodger FJ and Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441–1461

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Howitt SM, Harrison K and Badger MR (1993) Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC 7942 involved in carboxysome assembly and function. J Bacteriol 175:2871–2879

    PubMed  CAS  Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM and Tuker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101: 18228–18233

    Article  PubMed  CAS  Google Scholar 

  • Prommeenate P, Lennon AM, Markert C, Hippler M and Nixon PJ (2004) Subunit composition of NDH-1 complexes of Synechocystis sp. PCC 6803 - Identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex. J Biol Chem 279: 28165–28173

    Article  PubMed  CAS  Google Scholar 

  • Ramazanov Z, Rawat M, Henk MC, Mason CB, Matthews SW and Moroney JV (1995) The induction of the CO2-concentrating mechanism is correlated with the formation of the starch sheath around the pyrenoid of Chlamydomonas reinhardtii. Planta 195: 210–216

    Article  Google Scholar 

  • Ratti S, Giordano M and Morse D (2007) CO2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J Phycol. 43: 693–701

    Article  CAS  Google Scholar 

  • Rau GH, Takahashi T, and Des Marais DJ (1989) Latitudinal variations in plankton 13C: implications for CO2 and productivity in past oceans. Nature 341: 516–518

    Article  PubMed  CAS  Google Scholar 

  • Rau GH, Takahashi T, Des Marais DJ and Martin JH (1992) The relationship between delta 13C of organic matter and [CO2 (aq)] in ocean surface water: Data from a JGOFS site in the northeast Atlantic Ocean and a model. Geochim Cosmochim Acta 56: 1413–1419

    Article  PubMed  CAS  Google Scholar 

  • Raven JA (1991) Implications of inorganic C utilization: ecology, evolution and geochemistry. Can J Bot 69: 908–924

    Article  CAS  Google Scholar 

  • Raven JA (1994) Carbon fixation and carbon availability in marine phytoplankton. Photosynth Res 39: 259–273

    Article  CAS  Google Scholar 

  • Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27: 85–209

    Article  CAS  Google Scholar 

  • Raven JA (2003) Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynth Res 77: 155–171

    Article  PubMed  CAS  Google Scholar 

  • Raven JA, Ball LA, Beardal J, Giordano M and Maberly SC (2005) Algae lacking carbon concentrating mechanisms. Can J Bot 83: 879–890

    Article  CAS  Google Scholar 

  • Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Phil T R Soc B 303: 2641–2650

    Article  CAS  Google Scholar 

  • Raven JA, Johnston AM and Turpin DH (1993) Influence of changes in CO2 concentration and temperature on marine phytoplankton 13C/12C ratios: an analysis of possible mechanisms. Global Planet Change 8: 1–12

    Article  Google Scholar 

  • Reinfelder JR, Kraepiel AML and Morel FMM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996–999

    Article  PubMed  CAS  Google Scholar 

  • Reinfelder JR, Milligan AJ and Morel FMM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135: 2106–2111

    Article  PubMed  CAS  Google Scholar 

  • Reinhold L, Volokita M, Zenvirth D and Kaplan A (1984) Is HCO −3 transport in Anabaena a Na+-symport? Plant Physiol 76: 1090–1092

    Article  PubMed  CAS  Google Scholar 

  • Rexach J, Montero B, Fernandez E and Galvan A (1999) Differential regulation of the high affinity nitrite transport system III and IV in Chlamydomonas reinhardtii. J Biol Chem 274: 27801–27806

    Article  PubMed  CAS  Google Scholar 

  • Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60: 719–729

    Article  CAS  Google Scholar 

  • Riebesell U, Wolf-Gladrow D and Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361: 249–251

    Article  CAS  Google Scholar 

  • Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE and Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407: 364–367

    Article  PubMed  CAS  Google Scholar 

  • Roberts K, Granum E, Leegood RC and Raven JA (2007) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol 145: 230–235

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rochaix JD, Goldschmidt-Clermont M and Merchant S (eds) (1998) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, Advances in Photosy­nthesis, Vol 7, Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Rost B, Riebesell U, Burkhardt S and Sültemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48: 55–67

    Article  Google Scholar 

  • Rost B, Zondervan I and Riebesell U (2002) Light-dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi. Limnol Oceanogr 47: 120–128

    Article  CAS  Google Scholar 

  • Salon C, Mir NA and Canvin DT (1996) Influx and efflux of inorganic carbon in Synechococcus UTEX 625. Plant Cell Environ 19: 247–259

    Article  CAS  Google Scholar 

  • Satoh D, Hiraoka Y, Colman B and Matsuda Y (2001) Physiological and molecular biological characterization of intracellular carbonic anhydrase from the marine diatom Phaeodactylum tricornutum. Plant Physiol 126: 1459–1470

    Article  PubMed  CAS  Google Scholar 

  • Schulz KG, Rost B, Burkhardt S, Riebesell U, Thoms S and Wolf-Gladrow DA (2007) The effect of iron availability on the regulation of inorganic carbon acquisition in the coccolithophore Emiliania huxleyi and the significance of cellular compartmentation for stable carbon isotope fractionation. Geochim Cosmochim Acta 71: 5301–5312

    Article  CAS  Google Scholar 

  • Schwarz R, Lieman-Hurwitz J, Hassidim M and Kaplan A (1992) Phenotypic complementation of high-CO2-requiring mutants of the cyanobacterium Synechococcus sp. PCC 7942 by inosine 5’- monophosphate. Plant Physiol 100: 1987–1993

    Article  PubMed  CAS  Google Scholar 

  • Schwarz R, Reinhold L and Kaplan A (1995) Low activation state of ribulose 1,5-bisphosphate carboxylase/oxygenase in carboxysome-defective Synechococcus mutants. Plant Physiol 108: 183–190

    PubMed  CAS  Google Scholar 

  • Sekino K and Shiraiwa Y (1994) Accumulation and utilization of dissolved inorganic carbon by a marine unicellular coccolithophorid, Emiliania huxleyi. Plant Cell Physiol 35: 353–361

    CAS  Google Scholar 

  • Sharkey TD and Berry JA (1985) Carbon isotope fractionation in algae as influenced by inducible CO2 concentrating mechanism. In: Lucus WJ and Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. pp 339–401. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A and Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria. Function and phylogenetic analysis. J Biol Chem 277: 18658–18664

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A and Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: Genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Nat Acad Sci USA 98: 11789–11794

    Article  PubMed  CAS  Google Scholar 

  • Shiraiwa Y (2003) Physiological regulation of carbon fixation in the photosynthesis and calcification of coccolithophorids. Comp Biochem Physiol B-Biochem & Mol Biol 136: 775–783

    Article  CAS  Google Scholar 

  • Sippola K and Aro EM (1999) Thiol redox state regulates expression of psbA genes in Synechococcus sp. PCC 7942. Plant Mol Biol 41:425–433

    Article  PubMed  CAS  Google Scholar 

  • So AKC, Kassam A and Espie GS (1998) Na+-dependent HCO −3 transport in the cyanobacterium Synechocystis PCC6803. Can J Bot 76: 1084–1091

    CAS  Google Scholar 

  • Soupene E, Inwood W and Kustu S (2004) Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. Proc Natl Acad Sci USA 101: 7787–7792

    Article  PubMed  CAS  Google Scholar 

  • Spalding MH, Spreitzer RJ and Ogren WL (1983) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardtii. Plant Physiol 73: 273–276

    Article  PubMed  CAS  Google Scholar 

  • Steinke M, Evans C, Lee GA and Malin G (2007) Substrate kinetics of DMSP-lyases in axenic cultures and mesocosm populations of Emiliania huxleyi. Aquat Sci 69: 352–359

    Article  CAS  Google Scholar 

  • Sukenik A, Eshkol R, Livne A, Hadas O, Rom M, Tchernov D, Vardi A and Kaplan A (2002) Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnol Oceanogr 47:1656–1663

    Article  Google Scholar 

  • Sukenik A, Tchernov D, Huerta E, Lubian LM, Kaplan A and Livne A (1997) Uptake, efflux and photosynthetic utilization of inorganic carbon by the marine Eustigmatophyte nannochloropsis sp. J Phycol 33: 969–974

    Article  CAS  Google Scholar 

  • Suzuki K, Marek LF and Spalding MH (1990) A photorespiratory mutant of Chlamydomonas reinhardtii. Plant Physiol 93: 231–237

    Article  PubMed  CAS  Google Scholar 

  • Szabo E and Colman B (2007) Isolation and characterization of carbonic anhydrases from the marine diatom Phaeodactylum tricornutum. Physiol Plant 129: 484–492

    Article  CAS  Google Scholar 

  • Takahashi Y, Yamaguchi O and Omata T (2004) Roles of CmpR, a LysR family transcriptional regulator, in acclimation of the cyanobacterium Synechococcus sp. strain PCC 7942 to low-CO2 and high-light conditions. Mol Microbiol 52: 837–845

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Nakatsuma D, Harada H, Ishida M and 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: 207–217

    Article  PubMed  CAS  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M and Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101: 13531–13535

    Article  PubMed  CAS  Google Scholar 

  • Tchernov D, Hassidim M, Luz B, Sukenik A, Reinhold L and Kaplan A (1997) Sustained net CO2 evolution during photosynthesis by marine microorganisms. Curr Biol 7: 723–728

    Article  PubMed  CAS  Google Scholar 

  • Tchernov D, Helman Y, Keren N, Luz B, Ohad I, Reinhold L, Ogawa T and Kaplan A (2001) Passive entry of CO2 and its energy-dependent intracellular conversion to HCO −3 in cyanobacteria are driven by a photosystem I-generated ΔH+. J Biol Chem 276: 23450–23455

    Article  PubMed  CAS  Google Scholar 

  • Tchernov D, Silverman J, Luz B, Reinhold L and Kaplan A (2003) Massive light-dependent cycling of inorganic carbon between photosynthetic microorganisms and their surroundings. Photosynth Res 77: 95–103

    Article  PubMed  CAS  Google Scholar 

  • Tortell PD and Morel FMM (2002) Sources of inorganic carbon for phytoplankton in the eastern subtropical and equatorial pacific ocean. Limnol Oceanogr 47: 1012–1022

    Article  Google Scholar 

  • Tortell PD, DiTullio GR, Sigman PM and Morel FMM (2002) CO2 effects on taxonomic composition and nutrient utilization in an equatorial pacific phytoplankton assemblage. Marine Ecol Prog Ser 23: 37–43

    Article  Google Scholar 

  • Turkina MV, Blanco-Rivero A, Vainonen JP, Vener AV and Villarejo A (2006) CO2 limitation induces specific redox-dependent protein phosphorylation in Chlamydomonas reinhardtii. Proteomics 6: 2693–2704

    Article  PubMed  CAS  Google Scholar 

  • Tyrrell PN, Kandasamy RA, Crotty CM and Espie GS (1996) Ethoxyzolamide differentially inhibits CO2 uptake and Na+-independent and Na+-dependent HCO −3 uptake in the cyanobacterium Synechococcus sp. UTEX 625. Plant Physiol 112: 79–88

    PubMed  CAS  Google Scholar 

  • Van K and Spalding MH (1999) Periplasmic carbonic anhydrase structural gene (Cah1) mutant in Chlamydomonas reinhardtii. Plant Physiol 120: 757–64

    Article  PubMed  CAS  Google Scholar 

  • Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A and Levine A (1999) Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr Biol 9: 1061–1064

    Article  PubMed  CAS  Google Scholar 

  • Vardi A, Schatz D, Beeri K, Motro U, Sukenik A, Levine A and Kaplan A (2002) Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr Biol 12: 1767–1772

    Article  PubMed  CAS  Google Scholar 

  • Volokita M, Zenvirth D, Kaplan A and Reinhold L (1984) Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol 76: 599–602

    Article  PubMed  CAS  Google Scholar 

  • Wang HL, Postier BL and Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279: 5739–5751

    Article  PubMed  CAS  Google Scholar 

  • Wang Y and 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 

  • Woodger FJ, Badger MR and Price GD (2003) Inorganic carbon limitation induces transcripts encoding components of the CO2-concentrating mechanism in Synechococcus sp. PCC7942 through a redox-independent pathway. Plant Physiol 133: 2069–2080

    Article  PubMed  CAS  Google Scholar 

  • Woodger FJ, Bryant DA and Price GD (2005) Sensing of inorganic carbon limitation in Synechococcus PCC 7942 is correlated with the size of the internal inorganic carbon pool and involves oxygen. Plant Physiol 139:1959–1969

    Article  PubMed  CAS  Google Scholar 

  • Woodger FJ, Bryant DA and Price GD (2007) Transcriptional regulation of the CO2-concentrating mechanism in a euryhaline, coastal marine cyanobacterium, Synechococcus sp. Strain PCC 7002: role of NdhR/CcmR. J Bacteriol 189:3335–3347

    Article  PubMed  CAS  Google Scholar 

  • Xiang Y, Zhang J and 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 

  • Xu M, Bernát G, Singh G, Mi H, Rögner M, Pakrasi HB and Ogawa T (2008a) Properties of Mutants of Synechocystis sp. Strain PCC 6803 Lacking Carbon Sequestration Systems. Plant Cell Physiol 49: 1672–1677

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Ogawa T, Pakrasi HP and Mi H (2008b) Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium, Synechocystis sp. PCC 6803. Plant Cell Physiol 49: 994–997

    Article  PubMed  CAS  Google Scholar 

  • Yamano T, Miura K and 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 and 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

    Google Scholar 

  • Yoshioka S, Tanijuchi F, Miura K, Inoue T, Yamano T and Fukuzawa H (2004) The novel Myb transcription factor LCR1 regulates the CO2-response gene Cah1, encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Cell 16: 1466–1477

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Battchikova N, Jansen T, Appel J, Ogawa T and Aro EM (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp. PCC 6803. Plant Cell 16: 3326–3340

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi HB, Ogawa T and Aro EM (2005) Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem J 390: 513–520

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Sicora CI, Vorontsova N, Allahverdiyeva Y, Battchikova N, Nixon PJ and Aro EM (2007) FtsH protease is required for induction of inorganic carbon acquisition complexes in Synechocystis sp. PCC 6803. Mol Microbiol 65: 728–740

    Article  CAS  Google Scholar 

  • Zondervan I (2007) The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—A review. Deep Sea Research Part II: Topical Studies in Oceanography 54: 521–525

    Article  Google Scholar 

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Acknowledgements

This work was supported by grants to H.F. from the Japanese Ministry of Education, Science and Culture (Grants-in-Aid 170178020), to A.K. from the Israel Science Foundation (ISF), USA-Israel Science Foundation (BSF), European Commission (program Diatomics), the German-Israel Foundation (GIF) and the German BMBF and DFG, and to T.O. by the Membrane Biology EMSL Scientific Grand Challenge Project at the W.R. Wiley Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the U.S. Department of Energy Office of Biological and Environmental Research program located at Pacific Northwest National Laboratory. Pacific Northwest National Laboratory is operated for the Department of Energy by Battelle.

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Fukuzawa, H., Ogawa, T., Kaplan, A. (2012). The Uptake of CO2 by Cyanobacteria and Microalgae. In: Eaton-Rye, J., Tripathy, B., Sharkey, T. (eds) Photosynthesis. Advances in Photosynthesis and Respiration, vol 34. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1579-0_25

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