Abstract
Photosynthetic fixation of CO2 by cyanobacteria proceeds via the Calvin–Benson cycle. Its high efficiency is supported by the operation of the CO2-concentrating mechanism (CCM). The main constituents of CCM are the active transport and accumulation of the inorganic carbon (Сi) in the cytosol mainly in the form of HCO3 –, with its following transformation to CO2 in high concentration in a special microcompartment (carboxysome), containing ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). The presence of the CCM that functions before the Calvin–Benson cycle provides high CO2/O2 ratio in the vicinity of the primary CO2-fixing enzyme, Rubisco, to promote the carboxylation reaction and suppress the oxygenase reaction. To date, CCM is found in the cyanobacteria inhabiting different ecological niches. The structural composition of the CCM is different in α- and β-cyanobacteria, which main representatives belong correspondingly to seawater and freshwater habitats. Recently, the modulating CCM components have been detected in relict cyanobacteria, including that inhabiting saturated carbonate brine of soda lakes. This review focuses on various aspects of the carbon metabolism in cyanobacteria and interconversion of its organic and inorganic forms in the photosynthetic reactions of living cells. The comparison of ССМ physiology and biochemistry in the model and relict species of cyanobacteria is also highlighted. The evolutionary origin of CCM and the roles of CCM in the atmosphere formation and preservation of the ecology of Earth’s biosphere via the establishment of efficient mechanisms of CO2 acquisition are discussed.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- CA:
-
Carbonic anhydrase
- CCM:
-
CO2-concentrating mechanism (carbon-concentrating mechanism)
- Ci :
-
Inorganic carbon compounds (CO2 + HCO3 −)
- GAP:
-
Glyceraldehyde 3-phosphate
- High-CO2 cells:
-
Cells grown at 2–5% СО2
- Low-CO2 cells:
-
Cells grown under ambient atmospheric CO2 concentration (0.03–0.04%)
- PG:
-
2-Phosphoglycolate
- PGA:
-
3-Phosphoglyceric acid
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- RPP:
-
Reductive pentose phosphate (cycle/pathway)
- Rubisco:
-
Ribulose-1,5-bisphosphate carboxylase/oxygenase
- RuBP:
-
Ribulose-1,5-bisphosphate
- αKG:
-
α-Ketoglutarate
- К m :
-
Michaelis constant
- САМ:
-
Crassulacean acid metabolism
References
Aizawa К, Miyachi S (1986) Carbonic anhydrase and CO2-concentrating mechanism in microalgae and cyanobacteria. FEMS Microbiol Rev 39:215–233
Alber BE, Ferry JG (1994) A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci U S A 91:6909–6913
Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622
Badger MR, 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
Badger MR, Spalding MH (2000) CO2 acquisition, concentration and fixation in cyanobacteria and algae. In: Leegood RC, Sharkey TD, Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwer Academic Pubulications, Netherlands, pp 369–397
Badger MR, Kaplan A, Berry JA (1980) The internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a CO2 concentrating mechanism. Plant Physiol 66:407–413
Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336
Behrenfeld MJ, Randerson JT, McClain CR, Feldman GC, Los SO et al (2001) Biospheric primary production during an ENSO transition. Science 291:2594–2597
Bell LN (1985) Energetics of the photosynthesizing plant cell. University of Michigan, Harwood Academic Publishers. isbn:9783718601950
Benson AA, Bassham JA, Calvin M, Goudate TC, Haas UA, Sterka W (1950) The path of carbon in photosynthesis. Paper chromatography and radioautography of the products. J Am Chem Soc 12:1710–1718
Berner RA (2003) The long-term carbon cycle, fossil fuels and atmospheric composition. Nature 426:323–326
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
Brautigam A, Schliesky S, Kulahoglu C, Osborne CP, Weber AP (2014) Towards an integrative model of C4 photosynthetic subtypes: insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. J Exp Bot 65:3579–3593
Burnap RL, Hageman M, Kaplan A (2015) Regulation of CO2 concentrating mechanism in cyanobacteria. Life 5:348–371
Cai F, Dou Z, Bernstein SL, Leverenz R, Williams EB, Heinhorst S, Shively J, Cannon GC, Kerfeld CA (2015) Advances in understanding carboxysome assembly in Prochlorococcus and Synechococcus implicate CsoS2 as a critical component. Life 5:1141–1171
Cameron JC, Wilson SC, Bernstein SL, Kerfeld CA (2013) Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155:1131–1140
Cannon GC, Heinhorst S, Kerfeld CA (2010) Carboxysomal carbonic anhydrases: Structure and role in microbial CO2 fixation. Biochim Biophys Acta 1804:382–392
Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625–628
Cheng KH, Miller AG, Colman B (1972) An investigation of glycolate excretion in two species of blue-green algae. Planta 103:110–116
Cho SM, Jeoung SC, Song JY, Kupriyanova EV, Pronina NA, Lee BW, Jo SW, Park BS, Choi SB, Song JJ, Park YI (2015) Genomic survey and biochemical analysis of recombinant candidate cyanobacteriochromes reveals enrichment for near UV/Violet sensors in the halotolerant and alkaliphilic cyanobacterium Microcoleus IPPAS B353. J Biol Chem 290:28502–28514
Clement R, Dimnet L, Maberly SC, Gontero B (2016) The nature of the CO2-concentrating mechanisms in a marine diatom, Thalassiosira pseudonana. New Phytol 209:1417–1427
Coleman JR (1991) The molecular and biochemical analyses of CO2 concentrating mechanisms in cyanobacteria and microalgae. Plant Cell Environ 14:861–867
Cot SS, So AK, Espie GS (2008) A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. J Bacteriol 190:936–945
Daley SM, Kappell AD, Carrick MJ, Burnap RL (2012) Regulation of the cyanobacteria CO2-concentrating mechanism involves internal sensing of NADP+ and alpha-ketogutarate levels by transcription factor CcmR. PLoS One 7:e41286
Del Prete S, Vullo D, Fisher GM, Andrews KT, Poulsen SA, Capasso C, Supuran CT (2014) Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum – the η-carbonic anhydrases. Bioorg Med Chem Lett 24:4389–4396
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
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 alkaliphilic cyanobacterium Rhabdoderma lineare. Biochim Biophys Acta Bioenerg 1767(6):616–623
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
Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiotically to plants. Proc Natl Acad Sci U S A 105:17199–17204
Espie GS, Kimber MS (2011) Carboxysomes: cyanobacterial RubisCO comes in small packages. Photosynth Res 109:7–20
Folea IM, Zhang P, Nowaczyk MM, Ogawa T, Aro EM, 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
Fomina IR, Biel KY (2016) Photosynthetic carbon metabolism: strategy of adaptation over evolutionary history. In: Allakhverdiev SI (ed) Photosynthesis: new approaches to the molecular, cellular, and organismal levels. Scrivener Publishing LLC, pp 233–326
Gaudana SB, Zarzycki J, Moparthi VK, Kerfeld CA (2015) Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria. Photosynth Res 126:99–109
Georg J, Hess WR (2011) Cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286–300
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
Hackenberg C, Huege J, Engelhardt A, Wittink F, Laue M, Matthijs HC, Kopka J, Bauwe H, Hagemann M (2012) Low-carbon acclimation in carboxysome-less and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology 158:398–413
Hagemann M, Fernie AR, Espie GS, Kern R, Eisenhut M, Reumann S, Bauwe H, Weber AP (2013) Evolution of the biochemistry of the photorespiratory C2 cycle. Plant Biol (Stuttg) 15:639–647
Hagemann M, Kern R, Maurino VG, Hanson DT, Weber AP, Sage RF, Bauwe H (2016) Evolution of photorespiration from cyanobacteria to land plants, considering protein phylogenies and acquisition of carbon concentrating mechanisms. J Exp Bot 67:2963–2976
Hamilton TL, Bryant DA, Macalady JL (2016) The role of biology in planetary evolution: cyanobacterial primary production in low oxygen Proterozoic oceans. Environ Microbiol 18:325–340
Hammer A, Hodgson DR, Cann MJ (2006) Regulation of prokaryotic adenylyl cyclases by CO2. Biochem J 396:215–218
Hanson MR, Lin MT, Carmo-Silva AE, Parry MA (2016) Towards engineering carboxysomes into C3 plants. Plant J 87:38–50
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
Hewett-Emmett D, Tashian RE (1996) Functional diversity, conservation and convergence in the evolution of α-, β- and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5:50–77
Huege J, Goetze J, Schwarz D, Bauwe H, Hagemann M, Kopka J (2011) Modulation of the major paths of carbon in photorespiratory mutants of Synechocystis. PLoS One 6(1):e16278
Husic DW, Husic HD, Tolbert NE, Black CC (1987) The oxidative photosynthetic carbon cycle or C2 cycle. Crit Rev Plant Sci 5:45–100
Igamberdiev AU (2015) Control of Rubisco function via homeostatic equilibration of CO2 supply. Front Plant Sci 6:106
Igamberdiev AU, Roussel MR (2012) Feedforward non-Michaelis–Menten mechanism for CO2 uptake by Rubisco: contribution of carbonic anhydrases and photorespiration to optimization of photosynthetic carbon assimilation. Biosystems 107:158–166
Ingle RK, Colman B (1976) The relationship between carbonic anhydrase activity and glycolate excretion in the blue-green alga Coccochloris peniocystis. Planta 128:217–223
Johnston DT, Wolfe-Simon F, Pearson A, Knoll AH (2009) Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age. Proc Natl Acad Sci U S A 106:16925–16929
Kanzaki Y, Murakami T (2015) Estimates of atmospheric CO2 in the Neoarchean–Paleoproterozoic from paleosols. Geochim Cosmochim Acta 159:190–219
Kaplan A, Badger MR, Berry JA (1980) Photosynthesis and intracellular inorganic carbon pool in the blue-green algae Anabaena variabilis: response to external CO2 concentration. Planta 149:219–226
Kaplan A, Reinhold L (1999) CO2 concentrating mechanism in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50:539–570
Kaplan A, Zenvirth D, Marcus Y, Omata T, Ogawa T (1987) Energization and activation of inorganic carbon uptake by light in cyanobacteria. Plant Physiol 84:210–213
Kasting JF (2004) When methane made climate. Sci Am 291:78–85
Kern R, Eisenhut M, Bauwe H, Weber AP, Hagemann M (2013) Does the Cyanophora paradoxa genome revise our view on the evolution of photorespiratory enzymes? Plant Biol (Stuttg) 15:759–768
Khalifah RG (1971) The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 246:2561–2573
Kinney JN, Axen SD, Kerfeld CA (2011) Comparative analysis of carboxysome shell proteins. Photosynth Res 109:21–32
Klahn S, Orf I, Schwarz D, Matthiessen JKF, Kopka J, Hess WR, Hagemann M (2015) Integrated transcriptomic and metabolomic characterization of the low-carbon response using an ndhR mutant of Synechocystis sp. PCC 6803. Plant Physiol 169:1540–1556
Konhauser K (2009) Deepening the early oxygen debate. Nat Geosci 2:241–242
Kroth PG (2015) The biodiversity of carbon assimilation. J Plant Physiol 172:76–81
Kump LR (2008) The rise of atmospheric oxygen. Nature 451:277–278
Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los DA, Pronina N (2007) Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology 153:1149–1156
Kupriyanova EV, Cho SM, Park YI, Pronina NA, Los DA (2016) The complete genome of a cyanobacterium from a soda lake reveals the presence of the components of CO2-concentration mechanism. Photosynth Res 130:151–165
Kupriyanova EV, Samylina OS (2015) CO2-concentrating mechanism and its traits in haloalkaliphilic cyanobacteria. Microbiology (Moscow) 84:144–159
Kupriyanova EV, Sinetova MA, Cho SM, Park YI, Los DA, Pronina NA (2013) CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin. Photosynth Res 117:133–146
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
Liljas A, Laurber M (2000) A wheel invented three times. The molecular structures of the three carbonic anhydrases. EMBO Rep 1:16–17
Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74:1–20
Long BM, Badger MR, Whitney SM, Price GD (2007) Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282:29323–29335
Lyons TW, Reinhard CT, Planavsky NJ (2014) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506:307–315
Maddocks SE, Oyston PC (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609–3623
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
Marcus Y, Harel E, Kaplan A (1983) Adaptation of the cyanobacterium Anabaena variabilis to low CO2 concentration in their environment. Plant Physiol 71:208–210
McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol 164:2247–2261
McKenna R, Frost SC (2014) Overview of the carbonic anhydrase family. In: Frost SC, McKenna R (eds) Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications. Springer Dordrecht, Heidelberg, New York, London, pp 3–5
Mikhodyuk OS, Zavarzin GA, Ivanovsky RN (2008) Transport systems for carbonate in the extremely natronophilic cyanobacterium Euhalothece sp. Microbiology (Moscow) 77:412–418
Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda SI, 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
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 U S A 96:13571–13576
Omata T, Gohta S, Takahashi Y, Harano Y, Maeda S (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183:1891–1898
Orf I, Klahn S, Schwarz D, Frank M, Hess WR, Hagemann M, Kopka J (2015) Integrated analysis of engineered carbon limitation in a quadruple CO2/HCO3 − uptake mutant of Synechocystis sp. PCC 6803. Plant Physiol 169:1787–1806
Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29:379–414
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 U S A 107:2455–2460
Price GD (2011) Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth Res 109:47–57
Price GD, Badger MR, Woodger 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
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
Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci U S A 101:18228–18233
Rae BD, Long BM, Badger MR, Price GD (2013) Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77:357–379
Raines CA (2011) Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiol 155:36–42
Ramazanov Z, Pronina NA, Semenenko VE (1984) Oxygen-dependent induction of synthesis of the CO2-dependent soluble form of carbonic anhydrase in Chlorella cells. Sov Plant Physiol 31:448–455
Raven JA (1997) CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ 20:147–154
Raven JA, Beardall J (2016) The ins and outs of CO2. J Exp Bot 67:1–13
Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc Lond Ser B Biol Sci 363:2641–2650
Reinfelder JR, Kraepiel AM, Morel FM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407:996–999
Reinhold L, Zviman M, Kaplan A (1989) A quantitative model for inorganic carbon fluxes and photosynthesis in cyanobacteria. Plant Physiol 27:945–954
Schwarz D, Nodop A, Huge J, Purfurst S, Forchhammer K, Michel KP, Bauwe H, Kopka J, Hagemann M (2011) Metabolic and transcriptomic phenotyping of inorganic carbon acclimation in the cyanobacterium Synechococcus elongatus PCC 7942. Plant Physiol 155:1640–1655
Schwarz D, Orf I, Kopka J, Hagemann M (2013) Recent applications of metabolomics toward cyanobacteria. Metabolites 3:72–100
Scott KM, Henn-Sax M, Harmer TL, Longo DL, Frame CH, Cavanaugh CM (2007) Kinetic isotope effect and biochemical characterization of form IA RubisCO from the marine cyanobacterium Prochlorococcus marinus MIT9313. Limnol Oceanogr 52:2199–2204
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
Sergeev VN, Gerasimenko LM, Zavarzin GA (2002) The proterozoic history and present state of cyanobacteria. Microbiology (Moscow) 71:623–637
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
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 U S A 98:11789–11794
Smith KS, Ferry JG (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24:335–366
So АК, Van Spall НGС, Coleman JR, Espie ОS (1998) Catalytic exchange of 18O from 13С18О-labelled CO2 by wild type cells and есаА, есаВ, and ссаА mutants оf the cyanobacteria Synechococcus PCC7942 and Synechocystis PCC6803. Can J Bot 76:1153–1160
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
Stüeken EE, Buick R, Schauer AJ (2015) Nitrogen isotope evidence for alkaline lakes on late Archean continents. Earth Planet Sci Lett 411:1–10
Sültemeyer D, Klughammer В, Badger МR, Price GD (1998) Fast induction оf high affinity НСО3 − transport in cyanobacteria. Plant Physiol 116:183–192
Supuran CT (2008) Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7:168–181
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
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 U S A 103:7246–7251
Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737
Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414:543–546
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
Woodger FJ, Badger MR, 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
Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM (2008a) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61
Xu M, Ogawa T, Pakrasi HB, Mi H (2008b) Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium, Synechocystis sp. strain PCC6803. Plant Cell Physiol 49:994–997
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
Zavarzin GA (2008) Microbial biosphere. In: Dobretsov NL, Kolchanov NA, Rosanov AY, Zavarzin GA (eds) Biosphere origin and evolution. Springer, New York, pp 25–42
Zimmerman SA, Tomb JF, Ferry JG (2010) Characterization of CamH from Methanosarcina thermophila, founding member of a subclass of the γ-class of carbonic anhydrases. J Bacteriol 192:1353–1360
Acknowledgments
We thank Drs. M.A. Sinetova and A.G. Markelova (Institute of Plant Physiology, RAS, Moscow, Russia) for the TEM images of Arthrospira platensis IPPAS B-256 and Microcoleus sp. IPPAS B-353. We honor the memory of Dr. L.M. Gerasimenko who obtained image of Microcoleus calcification, kindly provided by Dr. O.S. Samylina (Institute of Microbiology, RAS, Moscow). E.V.K. was supported by a grant from Russian Science Foundation (no. 14-24-00020). A.U.I. was supported by a grant from the Natural Sciences and Engineering Research Council of Canada.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Pronina, N.A., Kupriyanova, E.V., Igamberdiev, A.U. (2017). Photosynthetic Carbon Metabolism and CO2-Concentrating Mechanism of Cyanobacteria. In: Hallenbeck, P. (eds) Modern Topics in the Phototrophic Prokaryotes. Springer, Cham. https://doi.org/10.1007/978-3-319-51365-2_8
Download citation
DOI: https://doi.org/10.1007/978-3-319-51365-2_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-51363-8
Online ISBN: 978-3-319-51365-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)