Skip to main content
SpringerLink
Log in

CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The cellular and molecular organization of the CO2-concentrating mechanism (CCM) of cyanobacteria is reviewed. The primary processes of uptake, translocation, and accumulation of inorganic carbon (Ci) near the active site of carbon assimilation by the enzyme ribulose-1,5-bisphosphate carboxylase in the C3 cycle in cyanobacteria are described as one of the specialized forms of CO2 concentration which occurs in some photoautotrophic cells. The existence of this form of CO2 concentration expands our understanding of photosynthetic Ci assimilation. The means of supplying Ci to the C3 cycle in cyanobacteria is not by simple diffusion into the cell, but it is the result of coordinated functions of high-affinity systems for the uptake of CO2 and bicarbonate, as well as intracellular CO2/HCO3 − interconversions by carbonic anhydrases. These biochemical events are under genetic control, and they serve to maintain cellular homeostasis and adaptation to CO2 limitation. Here we describe the organization of the CCM in cyanobacteria with a special focus on the CCM of relict halo- and alkaliphilic cyanobacteria of soda lakes. We also assess the role of the CCM at the levels of the organism, the biosphere, and evolution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

CA:

Carbonic anhydrase

CCM:

CO2-concentrating mechanism

Ci :

Inorganic carbon compounds (CO2 + HCO3 −)

High-CO2-cells:

Cells grown at 2–5 % CO2

K m :

Michaelis constant

Low-CO2-cells:

Cells grown under ambient atmospheric CO2 concentration (0.03–0.04 %)

PSII:

Photosystem II

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

TS:

Transport system

References

  • Aizawa K, Miyachi S (1986) Carbonic anhydrase and CO2-concentrating mechanism in microalgae and cyanobacteria. Fed Eur Microbiol Soc Microbiol Rev 39:215–233

    Article  CAS  Google Scholar 

  • Alber BE, Ferry JG (1996) Characterization of heterologously produced carbonic anhydrase from Methanosarcina thermophila. J Bacteriol 178:3270–3274

    PubMed  CAS  Google Scholar 

  • Arp G, Reimer A, Reitner J (2001) Photosynthesis-induced biofilm calcification and calcium concentrations in Phanerozoic oceans. Science 292:1701–1704. doi:10.1126/science.1057204

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Andrews TJ (1982) Photosynthesis and inorganic carbon usage by the marine cyanobacterium Synechococcus sp. Plant Physiol 70:517–523. doi:10.1104/pp.70.2.517

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622. doi:10.1093/jxb/erg076

    Article  PubMed  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. doi:10.1104/pp.66.3.407

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Hanson DT, Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29:161–173. doi:10.1071/PP01213

    Article  CAS  Google Scholar 

  • Badger M, Price GD, Long BM, Woodger FJ (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57:249–265. doi:10.1093/jxb/eri286

    Article  PubMed  CAS  Google Scholar 

  • Behrenfeld MJ, Randerson JT, McClain CR et al (2001) Biospheric primary production during an ENSO transition. Science 291:2594–2597. doi:10.1126/science.1055071

    Article  PubMed  CAS  Google Scholar 

  • Berner RA (2003) The long-term carbon cycle, fossil fuels and atmospheric composition. Nature 426:323–326. doi:10.1038/nature02131

    Article  PubMed  CAS  Google Scholar 

  • Blank CE, Sánchez-Baracaldo P (2010) Timing of morphological and ecological innovations in the cyanobacteria—a key to understanding the rise of atmospheric oxygen. Geobiology 8:1–23. doi:10.1111/j.1472-4669.2009.00220.x

    Article  PubMed  CAS  Google Scholar 

  • Briggs GE, Whittingham CP (1952) Factors affecting the rate of photosynthesis of Chlorella at low concentration of carbon dioxide and high illumination. New Phytol 51:236–249. doi:10.1111/j.1469-8137.1952.tb06130.x

    Article  CAS  Google Scholar 

  • Cannon GC, English RS, Shively JM (1991) In situ assay of ribulose-1,5-bisphosphate carboxylase/oxygenase in Thiobacillus neapolitanus. J Bacteriol 173:1565–1568

    PubMed  CAS  Google Scholar 

  • Cannon GC, Heinhorst S, Kerfeld CA (2010) Carboxysomal carbonic anhydrases: structure and role in microbial CO2 fixation. Biochim Biophys Acta 1804:382–392. doi:10.1016/j.bbapap.2009.09.026

    Article  PubMed  CAS  Google Scholar 

  • Cot SS, So AK, Espie GS (2008) A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. J Bacteriol 190:936–945. doi:10.1128/JB.01283-07

    Article  PubMed  CAS  Google Scholar 

  • De Simone G, Supuran CT (2012) (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 111:117–129. doi:10.1016/j.jinorgbio.2011.11.017

    Article  PubMed  Google Scholar 

  • Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC (2008) CO2 fixation kinetics of Halothiobacillus neapolitanus mutant carboxysomes lacking carbonic anhydrase suggest the shell acts as a diffusional barrier for CO2. J Biol Chem 283:10377–10384. doi:10.1074/jbc.M709285200

    Article  PubMed  CAS  Google Scholar 

  • Dubinin AV, Gerasimenko LM, Zavarzin GA (1995) Ecophysiology and species diversity of cyanobacteria from lake Magadi. Microbiology (Moscow) 64:717–721

    Google Scholar 

  • Dudoladova MV, Kupriyanova EV, Markelova AG, Sinetova MP, Allakhverdiev SI, Pronina NA (2007) The thylakoid carbonic anhydrase associated with photosystem II is the component of inorganic carbon accumulating system in cells of halo- and alkali-philic cyanobacterium Rhabdoderma lineare. Biochim Biophys Acta 1767:616–623. doi:10.1016/j.bbabio.2006.12.006

    Article  PubMed  CAS  Google Scholar 

  • Espie GS, Kimber MS (2011) Carboxysomes: cyanobacterial RubisCO comes in small packages. Photosynth Res 109:7–20. doi:10.1007/s11120-011-9656-y

    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. doi:10.1073/pnas.89.10.4437

    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. doi:10.1139/b98-070

    CAS  Google Scholar 

  • Gerasimenko LM, Mityushina LL, Namsaraev BB (2003) Microcoleus mats from alkaliphilic and halophilic communities. Microbiology (Moscow) 72:71–79. doi:10.1023/A:1022282124104

    Article  CAS  Google Scholar 

  • Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanism in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131. doi:10.1146/annurev.arplant.56.032604.144052

    Article  PubMed  CAS  Google Scholar 

  • Graham D, Reed ML (1971) Carbonic anhydrase and regulation of photosynthesis. Nat New Biol 231:81–83. doi:10.1038/newbio231081a0

    Article  PubMed  CAS  Google Scholar 

  • Heinhorst S, Williams EB, Cai F, Murin CD, Shively JM, Cannon GC (2006) Characterization of the carboxysomal carbonic anhydrase CsoSCA from Halothiobacillus neapolitanus. J Bacteriol 188:8087–8094. doi:10.1128/JB.00990-06

    Article  PubMed  CAS  Google Scholar 

  • Hogetsu D, Miyachi S (1979) Role of carbonic anhydrase in photosynthetic CO2 fixation in Chlorella. Plant Cell Physiol 20:747–756

    CAS  Google Scholar 

  • Igamberdiev AU, Kleczkowski LA (2011) Optimization of CO2 fixation in photosynthetic cells via thermodynamic buffering. BioSystems 103:224–229. doi:10.1016/j.biosystems.2010.10.001

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Badger MR, Berry JA (1980) Photosynthesis and the intracellular inorganic carbon pool in the blue-green alga Anabaena variabilis. Planta 149:219–226. doi:10.1007/BF00384557

    Article  CAS  Google Scholar 

  • Keeley JE, Rundel PW (2003) Evolution of CAM and C4 carbon-concentrating mechanisms. Int J Plant Sci 164:55–77

    Article  Google Scholar 

  • Konhauser K (2009) Deepening the early oxygen debate. Nat Geosci 2:241–242. doi:10.1038/ngeo484

    Article  CAS  Google Scholar 

  • 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. doi:10.1139/b91-136

    Article  CAS  Google Scholar 

  • Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los D, Pronina N (2007) Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology 153:1149–1156. doi:10.1099/mic.0.2006/003905-0

    Article  PubMed  CAS  Google Scholar 

  • Kupriyanova EV, Sinetova MA, Markelova AG, Allakhverdiev SI, Los DA, Pronina NA (2011) Extracellular β-class carbonic anhydrase of the alkaliphilic cyanobacterium Microcoleus chthonoplastes. J Photochem Photobiol, B 103:78–86. doi:10.1016/j.jphotobiol.2011.01.021

    Article  CAS  Google Scholar 

  • Liljas A, Laurberg M (2000) A wheel invented three times. The molecular structures of the three carbonic anhydrases. EMBO Rep 1:16–17. doi:10.1093/embo-reports/kvd016

    Article  PubMed  CAS  Google Scholar 

  • Long BM, Rae BD, Badger MR, Price GD (2011) Over-expression of the β-carboxysomal CcmM protein in Synechococcus PCC7942 reveals a tight co-regulation of carboxysomal carbonic anhydrase (CcaA) and M58 content. Photosynth Res 109:33–45. doi:10.1007/s11120-011-9659-8

    Article  PubMed  CAS  Google Scholar 

  • Maeda S, Badger MR, Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol Microbiol 43:425–435. doi:10.1046/j.1365-2958.2002.02753.x

    Article  PubMed  CAS  Google Scholar 

  • Marcus Y, Schwarz R, Friedberg D, Kaplan A (1986) High CO2 requiring mutants of Anacystis nidulans R2. Plant Physiol 82:610–612. doi:10.1104/pp.82.2.610

    Article  PubMed  CAS  Google Scholar 

  • Markelova AG, Sinetova MP, Kupriyanova EV, Pronina NA (2009) Distribution and functional role of carbonic anhydrase Cah3 associated with thylakoid in chloroplast and pyrenoid of Chlamydomonas reinhardtii. Russ J Plant Physiol 56:761–768. doi:10.1134/S1021443709060053

    Article  CAS  Google Scholar 

  • McKay RML, Gibbs SP (1991) Composition and function of pyrenoids: cytochemical and immunocytochemical approaches. Can J Bot 69:1040–1052. doi:10.1139/b91-134

    Article  CAS  Google Scholar 

  • Mikhodyuk OS, Zavarzin GA, Ivanovsky RN (2008) Transport systems for carbonate in the extremely natronophilic cyanobacterium Euhalothece sp. Microbiology (Moscow) 77:412–418. doi:10.1134/S002626170804005X

    Article  CAS  Google Scholar 

  • Miller AG, Colman B (1980) Evidence for HCO3 − transport by the blue-green alga (cyanobacterium) Coccochloris peniocystis. Plant Physiol 65:397–402. doi:10.1104/pp.65.2.397

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic anhydrase inhibitor on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183. doi:10.1104/pp.79.1.177

    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. doi:10.1104/pp.89.3.897

    Article  PubMed  CAS  Google Scholar 

  • Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 109:133–149. doi:10.1007/s11120-011-9635-3

    Article  PubMed  CAS  Google Scholar 

  • Nelson EB, Cenedella A, Tolbert NE (1969) Carbonic anhydrase levels in Chlamydomonas. Phytochemistry 8:2305–2306. doi:10.1016/S0031-9422(00)88144-3

    Article  CAS  Google Scholar 

  • Ogawa T (1990) Mutants of Synechocystis PCC6803 in inorganic carbon transport. Plant Physiol 94:760–765. doi:10.1104/pp.94.2.760

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC7942. Proc Natl Acad Sci USA 96:13571–13576. doi:10.1073/pnas.96.23.13571

    Article  PubMed  CAS  Google Scholar 

  • Palenik B, Brahamsha B, Larimer FW et al (2003) The genome of a motile marine Synechococcus. Nature 424:1037–1042. doi:10.1038/nature01943

    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 Let. 444:102–105. doi:10.1016/S0014-5793(99)00037-X

    Article  CAS  Google Scholar 

  • Peña KL, Castel SE, de Araujo C, Espie GS, Kimber MS (2010) Structural basis of the oxidative activation of the carboxysomal gamma-carbonic anhydrase, CcmM. Proc Natl Acad Sci USA 107:2455–2460. doi:10.1073/pnas.0910866107

    Article  PubMed  Google Scholar 

  • Price GD (2011) Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth Res 109:47–57. doi:10.1007/s11120-010-9608-y

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Badger MR (1989a) Isolation and characterization of high CO2-requiring-mutants of the cyanobacterium Synechococcus PCC7942. Two phenotypes that accumulate inorganic carbon but are apparently unable to generate CO2 within the carboxysomes. Plant Physiol 91:514–525. doi:10.1104/pp.91.2.514

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Badger MR (1989b) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-requiring phenotype. Evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol 91:505–513. doi:10.1104/pp.91.2.505

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Coleman JR, Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100:784–793. doi:10.1104/pp.100.2.784

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Sültemeyer D, Klughammer B, Ludwig M, Badger MR (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins and recent advances. Can J Bot 76:973–1002. doi:10.1139/b98-081

    CAS  Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101:18228–18233. doi:10.1073/pnas.0405211101

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Badger MR, Wodger FJ, 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. doi:10.1093/jxb/erm112

    Article  PubMed  CAS  Google Scholar 

  • Pronina NA (2000) The organization and physiological role of the CO2 concentrating mechanisms in microalgal photosynthesis. Russ J Plant Physiol 47:706–714

    CAS  Google Scholar 

  • Pronina NA, Semenenko VE (1984) Localization of membrane-associated and soluble forms of carbonic anhydrase in Chlorella cells. Sov Plant Physiol 31:187–196

    Google Scholar 

  • Pronina NA, Semenenko VE (1992) Role of the pyrenoid in concentration, generation and fixation of CO2 in the chloroplast of microalgae. Sov Plant Physiol 39:470–476

    Google Scholar 

  • Pronina NA, Avramova S, Georgiev D, Semenenko VE (1981) A pattern of carbonic anhydrase activity in Chlorella and Scenedesmus on cell adaptation to high light intensity and low CO2 concentration. Sov Plant Physiol 28:32–40

    Google Scholar 

  • Rabinowitch EI (1945) Photosynthesis and related processes, vol 1. Interscience Publishers, New York

    Book  Google Scholar 

  • Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc Lond B Biol Sci 363:2641–2650. doi:10.1098/rstb.2008.0020

    Article  PubMed  CAS  Google Scholar 

  • Raven JA, Giordano M, Beardall J, Maberly SC (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philos Trans R Soc Lond B Biol Sci 367:493–507. doi:10.1098/rstb.2011.0212

    Article  PubMed  CAS  Google Scholar 

  • Reinhold L, Zviman M, Kaplan A (1989) A quantitative model for inorganic carbon fluxes and photosynthesis in cyanobacteria. Plant Physiol 27:945–954

    CAS  Google Scholar 

  • Sasaki T, Pronina N, Maeshima M, Iwasaki L, Kurano N, Miyachi S (1999) Development of vacuoles and vacuolar ATPase activity under extremely high-CO2 conditions in Chlorococcum littorale II. Plant Biol 1:68–75. doi:10.1111/j.1438-8677.1999.tb00710.x

    Article  CAS  Google Scholar 

  • Sawaya MR, Cannon GC, Heinhorst S, Tanaka S, Williams EB, Yeates TO, Kerfeld CA (2006) The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J Biol Chem 281:7546–7555. doi:10.1074/jbc.M510464200

    Article  PubMed  CAS  Google Scholar 

  • Sergeenko TV, Muradyan EA, Pronina NA, Klyachko-Gurvich GL, Mishina IM, Tsoglin LN (2000) The effect of extremely high CO2 concentration on the growth and biochemical composition of microalgae. Russ J Plant Physiol 47:632–638

    CAS  Google Scholar 

  • Sergeev VN, Gerasimenko LM, Zavarzin GA (2002) The proterozoic history and present state of cyanobacteria. Microbiology (Moscow) 71:623–637. doi:10.1023/A:1021415503436

    Article  CAS  Google Scholar 

  • Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, 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 Natl Acad Sci USA 98:11789–11794. doi:10.1073/pnas.191258298

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria. Function and phylogenetic analysis. J Biol Chem 277:18658–18664. doi:10.1074/jbc.M112468200

    Article  PubMed  CAS  Google Scholar 

  • Sinetova MA, Kupriyanova EV, Markelova AG, Allakhverdiev SI, Pronina NA (2012) Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii. Biochim Biophys Acta 1817:1248–1255. doi:10.1016/j.bbabio.2012.02.014

    Article  PubMed  CAS  Google Scholar 

  • Smith KS, Ferry JG (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24:335–366. doi:10.1111/j.1574-6976.2000.tb00546.x

    Article  PubMed  CAS  Google Scholar 

  • So AK, Espie GS (1998) Cloning, characterization and expression carbonic anhydrase from the cyanobacterium Synechocystis PCC6803. Plant Mol Biol 37:205–215. doi:10.1023/A:1005959200390

    Article  PubMed  CAS  Google Scholar 

  • So AK, Van Spall HGC, Coleman JR, Espie OS (1998) Catalytic exchange of 18O from 13C18O-labelled CO2 by wild type cells and ecaA, ecaB, and ccaA mutants of the cyanobacteria Synechococcus PCC7942 and Synechocystis PCC6803. Can J Bot 76:1153–1160

    CAS  Google Scholar 

  • Soltes-Rak E, Mulligan ME, Coleman JR (1997) Identification and characterization of 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) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardtii. Plant Physiol 73:273–276. doi:10.1104/pp.73.2.273

    Article  PubMed  CAS  Google Scholar 

  • Tabita FR, Satagopan S, Hanson TE, Kreel NE, Scott SS (2008) Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. J Exp Bot 59:1515–1524. doi:10.1093/jxb/erm361

    Article  PubMed  CAS  Google Scholar 

  • Tcherkez GG, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103:7246–7251. doi:10.1073/pnas.0600605103

    Article  PubMed  CAS  Google Scholar 

  • Wang HL, Postier BL, 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. doi:10.1074/jbc.M311336200

    Article  PubMed  CAS  Google Scholar 

  • Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM (2008) Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 6:681–691. doi:10.1038/nrmicro1913

    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. doi:10.1104/pp.100.2.794

    Article  PubMed  CAS  Google Scholar 

  • Zavarzin GA (1997) The rise of the biosphere. Microbiology (Moscow) 66:603–611

    CAS  Google Scholar 

  • Zavarzin GA (2008) Microbial Biosphere. In: Dobretsov NL, Kolchanov NA, Rosanov AY, Zavarzin GA (eds) Biosphere origin and evolution. Springer Science + Business Media, LLC., New York, pp 25–42

    Chapter  Google Scholar 

Download references

Acknowledgments

We honor the memory of Georgy A. Zavarzin, who initiated the study of the CCM in the relict cyanobacteria. This work was supported by the Grants from Russian Foundation for Basic Research (nos. 13-04-00193, 12-04-32148, and 12-04-00473), and by the Grant from the “Molecular and Cell Biology” program of the Russian Academy of Sciences. Y.-I. Park was supported by the Grants from the Next-Generation BioGreen 21 Program, Rural Development Administration (PJ8205) and from Advanced Biomass Research and Development Center, Republic of Korea (2011-0031344).

Author information

Authors and Affiliations

  1. Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street, 35, Moscow, 127276, Russia

    Elena V. Kupriyanova, Maria A. Sinetova, Dmitry A. Los & Natalia A. Pronina

  2. Department of Biological Sciences, College of Biological Sciences and Biotechnology, Chungnam National University, Daejeon, 305-764, Republic of Korea

    Sung Mi Cho & Youn-Il Park

Authors
  1. Elena V. Kupriyanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria A. Sinetova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sung Mi Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Youn-Il Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dmitry A. Los
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Natalia A. Pronina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalia A. Pronina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kupriyanova, E.V., Sinetova, M.A., Cho, S.M. et al. CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin. Photosynth Res 117, 133–146 (2013). https://doi.org/10.1007/s11120-013-9860-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9860-z

Keywords

Search

Navigation