Skip to main content
SpringerLink
Log in

Regulatory components of carbon concentrating mechanisms in aquatic unicellular photosynthetic organisms

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

This review provides an insight into the regulation of the carbon concentrating mechanisms (CCMs) in lower organisms like cyanobacteria, proteobacteria, and algae. CCMs evolved as a mechanism to concentrate CO2 at the site of primary carboxylating enzyme Ribulose-1, 5-bisphosphate carboxylase oxygenase (Rubisco), so that the enzyme could overcome its affinity towards O2 which leads to wasteful processes like photorespiration. A diverse set of CCMs exist in nature, i.e., carboxysomes in cyanobacteria and proteobacteria; pyrenoids in algae and diatoms, the C4 system, and Crassulacean acid metabolism in higher plants. Prime regulators of CCM in most of the photosynthetic autotrophs belong to the LysR family of transcriptional regulators, which regulate the activity of the components of CCM depending upon the ambient CO2 concentrations. Major targets of these regulators are carbonic anhydrase and inorganic carbon uptake systems (CO2 and HCO3 − transporters) whose activities are modulated either at transcriptional level or by changes in the levels of their co-regulatory metabolites. The article provides information on the localization of the CCM components as well as their function and participation in the development of an efficient CCM. Signal transduction cascades leading to activation/inactivation of inducible CCM components on perception of low/high CO2 stimuli have also been brought into picture. A detailed study of the regulatory components can aid in identifying the unraveled aspects of these mechanisms and hence provide information on key molecules that need to be explored to further provide a clear understanding of the mechanism under study.

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

References

  • Aichi M, Takatani N, Omata T (2001) Role of NtcB in activation of nitrate assimilation genes in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183:5840–5847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59(7):1555–1568

    Article  CAS  PubMed  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  PubMed  Google Scholar 

  • Atkinson N, Feike D, Mackinder LC, Meyer MT, Griffiths H, Jonikas MC et al (2016) Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnol. 14:1302–1315

    Article  CAS  Google Scholar 

  • Badger MR, Bek EJ (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59:1525–1541

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76:1052–1071

    CAS  Google Scholar 

  • Baker SH, Williams DS, Aldrich HC, Gambrell AC, Shively JM (2000) Identification and localization of the carboxysome peptide CsoS3 and its corresponding gene in Thiobacillus neapolitanus. Arch Microbiol 173:278–283

    Article  CAS  PubMed  Google Scholar 

  • Blanco-Rivero A, Shutova T, Román MJ, Villarejo A, Martinez F (2012) Phosphorylation controls the localization and activation of the lumenal carbonic anhydrase in Chlamydomonas reinhardtii. PLoS One 7:e49063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bock R (2007) Structure, function, and inheritance of plastid genomes. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin, pp 29–63

    Chapter  Google Scholar 

  • Brueggeman AJ, Gangadharaiah DS, Cserhati MF, Casero D, Weeks DP, Ladunga I (2012) Activation of the carbon concentrating mechanism by CO2 deprivation coincides with massive transcriptional restructuring in Chlamydomonas reinhardtii. Plant Cell. 24:1860–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burnap RL, Hagemann M, Kaplan A (2015) Regulation of CO2 concentrating mechanism in cyanobacteria. Life. 5:348–371

    Article  PubMed  PubMed Central  Google Scholar 

  • Burow M, Chen Z, Mouton T, Moroney J (1996) Isolation of cDNA clones of genes induced upon transfer of Chlamydomonas reinhardtii cells to low CO2. Plant Mol Biol 31:443–448

    Article  CAS  PubMed  Google Scholar 

  • Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM (2001) Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl Environ Microbiol 67:5351–5361

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Daley SME, Kappell AD, Carrick MJ, Burnap RL (2012) Regulation of the cyanobacterial CO2-concentrating mechanism involves internal sensing of NADP+ and α-ketogutarate levels by transcription factor CcmR. PLoS One 7:e41286. doi:10.1371/journal.pone.0041286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dangel AW, Tabita FR (2015) CbbR, the master regulator for microbial carbon dioxide fixation. J Bacteriol 197(22):3488–3498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobrinski KP, Boller AJ, Scott KM (2010) Expression and function of four carbonic anhydrase homologous in the deep-sea chemolithoautotroph Thiomicrospira crunogena. Appl Environ Microbiol 76:3561–3567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobrinski KP, Enkemann SA, Yoder SJ, Haller E, Scott KM (2012) Transcriptional response of the sulfur chemolithoautotroph Thiomicrospira crunogena to dissolved inorganic carbon limitation. J Bacteriol 194:2074–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du J, Förster B, Rourke L, Howitt SM, Price GD (2014) Characterisation of cyano-bacterial bicarbonate transporters in E. coli shows that SbtA homologs are functional in this heterologous expression system. PLoS One 9:e115905. doi:10.1371/journal.pone.0115905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duanmu D, Miller AR, Horken KM, Weeks DP, Spalding MH (2009) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubbs JM, Tabita FR (2004) Regulators of nonsulfur purple phototrophic bacteria and the interactive control of CO2 assimilation, nitrogen fixation, hydrogen metabolism and energy generation. FEMS Microbiol Rev 28:353–376

    Article  CAS  PubMed  Google Scholar 

  • Fang W, Si Y, Casero D, Merchant SS, Pellegrini M, Ladunga I, Liu P, Spalding MH (2012) Transcriptome-wide changes in Chlamydomonas gene expression regulated by carbon dioxide and the CO2 concentrating mechanism regulator CIA5/CCM1. Plant Cell. 24:1876–1893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuzawa H, Miura K, Ishizaki K, Kucho KI, Saito T, Kohinata T, Ohyama K (2001) Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proc Natl Acad Sci USA 98:5347–5352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galván A, Rexach J, Mariscal V, Fernández E (2002) Nitrite transport to the chloroplast in Chlamydomonas reinhardtii: molecular evidence for a regulated process. J Exp Bot 53:845–853

    Article  PubMed  Google Scholar 

  • Gao H, Wang Y, Fei X, Wright DA, Spalding MH (2015) Expression activation and functional analysis of HLA3, a putative inorganic carbon transporter in Chlamydomonas reinhardtii. Plant J. 82:1–11

    Article  CAS  PubMed  Google Scholar 

  • Harada H, Nakatsuma D, Ishida M, 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  CAS  PubMed  PubMed Central  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(23):8087–8094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Im CS, Grossman AR (2001) Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. Plant J. 30:301–313

    Article  Google Scholar 

  • Ishii A, Hihara Y (2008) An AbrB-like transcriptional regulator, Sll 0822, is essential for the activation of nitrogen-regulated genes in Synechocystis sp. PCC 6803. Plant Physiol 148:660–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jäger-Vottero P, Dorne AJ, Jordanov J, Douce R, Joyard J (1997) Redox chains in the chloroplast envelope membranes: spectroscopic evidence for the presence of electron carriers, including iron-sulfur centers. Proc Natl Acad Sci 94:1597–1602

    Article  PubMed  PubMed Central  Google Scholar 

  • Joshi GS, Romagnoli S, Verberkmoes NC, Hettich RL, Pelletier D, Tabita FR (2009) Differential accumulation of form I Rubisco in Rhodopseudomonas palustris CGA010 under photoheterotrophic growth conditions with reduced carbon sources. J Bacteriol 191:4243–4250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi GS, Bobst CE, Tabita FR (2011) Unravelling the regulatory twist—regulation of CO2 fixation in Rhodopseudomonas palustris CGA010 mediated by atypical response regulator(s). Mol Microbiol 80:756–771

    Article  CAS  PubMed  Google Scholar 

  • Joshi GS, Zianni M, Bobst CE, Tabita FR (2013) Regulatory twist and synergistic role of metabolic coinducer- and response regulator-mediated CbbR-cbb(I) interactions in Rhodopseudomonas palustris CGA010. J Bacteriol 195:1381–1388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalloniati C, Tsikou D, Lampiri V, Fotelli MN, Rennenberg H, Chatzipavlidis I, Fasseas C, Katinakis P, Flemetakis E (2009) Characterization of a Mesorhizobium lotiα-type carbonic anhydrase and its role in symbiotic nitrogen fixation. J Bacteriol 191:2593–2600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan A (2017) On the cradle of CCM research: discovery, development, and challenges ahead. J Exp Bot. doi:10.1093/jxb/erx122

    PubMed  Google Scholar 

  • Kaplan A, Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Biol 50:539–559

    Article  CAS  Google Scholar 

  • Katoh A, Lee KS, Fukuzawa H, Ohyama K, Ogawa T (1996) A cemA homologue essential to CO2 transport in the cyanobacterium, Synechocystis PCC6803. Proc Natl Acad Sci USA 93:4006–4010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kikuchi H, Aichi M, Suzuki I, Omata T (1996) Positive regulation by nitrite of the nitrate assimilation operon in the cyanobacteria Synechococcus sp. strain PCC 7942 and Plectonema boryanum. J Bacteriol 178:5822–5825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinney JN, Axen SD, Kerfeld CA (2011) Comparative analysis of carboxysome shell proteins. Photosynth Res 109:21–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580(4):1112–1122

    Article  CAS  PubMed  Google Scholar 

  • Kroth PG (2015) The biodiversity of carbon assimilation. Plant Physiol 172:76–81

    Article  CAS  Google Scholar 

  • Kroth PG, Chiovitti A, Gruber A, Martin-Jezequel V, Mock T, Parker MS, Stanley MS, Kaplan A, Caron L, Weber T, Maheswari U, Armbrust EV, Bowler C (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3:e1426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusian B, Bowien B (1997) Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 21:135–155

    Article  CAS  PubMed  Google Scholar 

  • Lawand S, Dorne AJ, Long D, Coupland G, Mache R, Carol P (2002) Arabidopsis A BOUT DE SOUFFLE, which is homologous with mammalian carnitine acyl carrier, is required for postembryonic growth in the light. Plant Cell. 14:2161–2173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieman-Hurwitz J, Haimovich M, Shalev-Malul G, Ishii A, Hihara Y et al (2009) A cyanobacterial AbrB-like protein affects the apparent photosynthetic affinity for CO2 by modulating low-CO2-induced gene expression. Environ Microbiol 11:927–936

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Long BM, Tucker L, Badger MR, Price GD (2010) Functional cyanobacterial β-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153(1):285–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lü W, Du J, Schwarzer NJ, Wacker T, Andrade SLA, Einsle O (2013) The formate/nitrite transporter family of anion channels. Biol Chem 394:715–727

    Article  PubMed  CAS  Google Scholar 

  • Mackinder LC, Meyer MT, Mettler-Altmann T, Chen VK, Mitchell MC, Caspari O, Freeman Rosenzweig ES, Pallesen L, Reeves G, Itakura A, Roth R, Sommer F, Geimer S, Mühlhaus T, Schroda M et al (2016) A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle. Proc Natl Acad Sci USA 113:5958–5963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maddocks SE, Oyston PC (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609–3623

    Article  CAS  PubMed  Google Scholar 

  • Maier UG, Fraunholz M, Zauner S, Penny S, Douglas S (2000) A nucleomorph-encoded CbbX and the phylogeny of Rubisco regulators. Mol Biol Evol 17:576–583

    Article  CAS  PubMed  Google Scholar 

  • Marcus EA, Moshfegh AP, Sachs G, Scott DR (2005) The periplasmic carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J Bacteriol 187:729–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuda Y, Kroth PG (2014) Carbon fixation in diatoms. In: Hohmann-Marriott MF (ed) The structural basis of biological energy generation, advances in photosynthesis and respiration, vol 39, pp 335–362

  • Matsuda Y, Harada H, Nakajima K, Colman B (2007) Sensing of elevating CO2 in a marine diatom: molecular mechanisms and implications. Plant Signal Behav 2(2):109–111

    Article  PubMed  PubMed Central  Google Scholar 

  • McGinn PJ, Price GD, Maleszka R, 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 PCC6803. Plant Physiol 132:218–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meijer WG (1994) The Calvin cycle enzyme phosphoglycerate kinase of Xanthobacter flavus required for autotrophic CO2 fixation is not encoded by the cbb operon. J Bacteriol 176:6120–6126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meijer WG, vanden Bergh ERE, Smith LM (1996) Induction of the gap-pgk operon encoding glyceraldehyde-3-phosphate dehydrogenase and 3-phosphoglycerate kinase of Xanthobacter flavus requires the LysR-type transcriptional activator CbbR. J Bacteriol 178:881–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer MT, Genkov T, Skepper JN, Jouhet J, Mitchell MC, Spreitzer RJ, Griffiths H (2012) RuBisCO small-subunit α-helices control pyrenoid formation in Chlamydomonas. Proc Nat Acad Sci USA 109:19474–19479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minoda A, Weber AP, Tanaka K, Miyagishima SY (2010) Nucleus-independent control of the Rubisco operon by the plastid-encoded transcription factor Ycf30 in the red alga Cyanidioschyzon merolae. Plant Physiol 154:1532–1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell MC, Meyer MT, Griffiths H (2014) Dynamics of carbon-concentrating mechanism induction and protein Relocalization during the dark-to-light transition in Synchronized Chlamydomonas reinhardtii. Plant Physiol 166:1073–1082

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT et al (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Moroney JV, Somanchi A (1999) How do algae concentrate CO2 to increase the efficiency of photosynthetic carbon fixation? Plant Physiol 119:9–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nakajima K, Tanaka A, Matsuda Y (2013) SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc Natl Acad Sci 110:1767–1772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda S, 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  CAS  PubMed  Google Scholar 

  • Ohashi Y, Shi W, Takatani N, Aichi M, Maeda S, Watanabe S, Yoshikawa H, Omata T (2011) Regulation of nitrate assimilation in cyanobacteria. J Exp Bot 62(4):1411–1424

    Article  CAS  PubMed  Google Scholar 

  • Ohno N, Inoue T, Yamashiki R, Nakajima K, Kitahara Y, Ishibashi M, Matsuda Y (2012) CO2-cAMP-responsive cis-elements targeted by a transcription factor with CREB/ATF-like basic zipper domain in the marine diatom Phaeodactylum tricornutum. Plant Physiol 158:499–513

    Article  CAS  PubMed  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 PCC 7942. Proc Natl Acad Sci USA 96:13571–13576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orf I, Schwarz D, Kaplan A, Kopka J, Hess WR, Hagemann M, Klähn S (2016) CyAbrB2 contributes to the transcriptional regulation of low CO2 acclimation in Synechocystis sp. PCC 6803. Plant Cell Physiol 57:2232–2243

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Petersen TN, Brunak S, Gunnar von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Pollock SV, Prout DL, Godfrey AC, Lemaire SD, 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  CAS  PubMed  Google Scholar 

  • Price GD, Howitt SM, Harrison K, Badger MR (1993) Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. J Bacteriol 175:2871–2879

    Article  CAS  PubMed  PubMed Central  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

    CAS  Google Scholar 

  • Price GD, Maeda SI, Omata T, Badger MR (2002) Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942. Funct Plant Biol 29:131–149

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Price GD, Badger MR, vonCaemmerer S (2011) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:20–26

    Article  CAS  PubMed  Google Scholar 

  • Puskas L, Inui M, Zahn K, Yukawa H (2000) A periplasmic, alpha type carbonic anhydrase from Rhodopseudomonas palustris is essential for bicarbonate uptake. Microbiology 146:2957–2966

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raven JA (2006) Sensing inorganic carbon: CO2 and HCO3 −. Biochem J 396:e5–e7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reith ME (1995) Molecular biology of rhodophyte and chromophyte plastids. Annu Rev Plant Physiol Mol Biol 46:549–575

    Article  CAS  Google Scholar 

  • Rolland N, Dorne AJ, Amoroso G, Sultemeyer DF, Joyard J, Rochaix JD (1997) Disruption of the plastid ycf10 open reading frame affects uptake of inorganic carbon in the chloroplast of Chlamydomonas. EMBO J 16:6713–6726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romagnoli S, Tabita FR (2007) Phosphotransfer reactions of the CbbRRS three-protein two- component system from Rhodopseudomonas palustris CGA010 appear to be controlled by an internal molecular switch on the sensor kinase. J Bacteriol 189:325–335

    Article  CAS  PubMed  Google Scholar 

  • Sage RF (2002) How terrestrial organisms sense, signal and respond to carbon dioxide. Integr Comp Biol 42:469–480

    Article  PubMed  Google Scholar 

  • Sasaki Y, Sekiguchi K, Nagano Y, Matsuno R (1993) Chloroplast envelope protein encoded by chloroplast genome. FEBS Lett 316(1):93–98

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626

    Article  CAS  PubMed  Google Scholar 

  • Scott KM, Sievert SM, Abril FN, Ball LA, Barrett CJ, Blake RA, Boller AJ, Chain PS, Clark JA, Davis CR (2006) The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2. PLoS Biol 4(12):e383. doi:10.1371/journal.pbio.0040383

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sonoda M, Katoh H, Vermaas W, Schmetterer G, Ogawa T (1998) Photosynthetic electron transport involved in pxcA dependent proton extrusion in Synechocystis sp. strain PCC6803: effect of pxcA inactivation on CO2, HCO3 −, and NO3 uptake. J Bacteriol 180:3799–3803

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spalding MH (1998) CO2 acquisition: adaptation to changing carbon availability. In: Rochaix JD et al (eds) The molecular biology of chloroplasts and mitochondria in chlamydomonas. Kluwer Academic Publishers, Dordrecht, pp 529–547

    Google Scholar 

  • Spalding MH (2008) Microalgal carbon-dioxide-concentrating mechanisms: chlamydomonas inorganic carbon transporters. J Exp Bot 59:1463–1473

    Article  CAS  PubMed  Google Scholar 

  • Spalding MH, Jeffrey M (1989) Membrane-associated polypeptides induced in Chlamydomonas by limiting CO2 concentrations. Plant Physiol 89:133–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki I, Kikuchi H, Nakanishi S, Fujita Y, Sugiyama T, Omata T (1995) A novel nitrite reductase gene from the cyanobacterium Plectonema boryanum. J Bacteriol 177:6137–6143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tachibana M, Allen AE, Kikutani S, Endo Y, Bowler C, Matsuda Y (2011) Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth Res 109:205–221

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Yamaguchi O, Omata T (2004) Roles of CmpR, a LysR family transcriptional regulator, in acclimation of the cyanobacterium Synechococcus sp. strain PCC 7942 to low-CO(2) and high-light conditions. Mol Microbiol 52:837–845

    Article  CAS  PubMed  Google Scholar 

  • Tanaka A, Ohno N, Nakajima K, Matsuda Y (2016) Light and CO2/cAMP signal cross talk on the promoter elements of chloroplastic β-carbonic anhydrase genes in the marine diatom Phaeodactylum tricornutum. Plant Physiol 170:1105–1116

    Article  CAS  PubMed  Google Scholar 

  • Taylor TC, Backlund A, Bjorhall K, Spreitzer RJ, Andersson I (2001) First crystal structure of Rubisco from a green alga, Chlamydomonas reinhardtii. J Biol Chem 276(51):48159–48164

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tirumani S, Kokkanti M, Chaudhari V, Shukla M, Rao BJ (2014) Regulation of CCM genes in Chlamydomonas reinhardtii during conditions of light–dark cycles in synchronous cultures. Plant Mol Biol 85:277–286

    Article  CAS  PubMed  Google Scholar 

  • Tomar V, Sidhu GK, Nogia P, Mehrotra R, Mehrotra S (2016) Role of habitat and great oxidation event on the occurrence of three multisubunit inorganic carbon-uptake systems in cyanobacteria. J Genet 95:109–118

    Article  CAS  PubMed  Google Scholar 

  • vanKeulen G, Girbal L, van den Bergh ERE, Dijkhuizen L, Meijer WG (1998) The LysR-type transcriptional regulator CbbR controlling autotrophic CO2 fixation by Xanthobacter flavus is an NADPH sensor. J Bacteriol 180:1411–1417

    CAS  Google Scholar 

  • vanKeulen G, Dijkhuizen L, Meijer WG (2000) Effects of the Calvin cycle on the nicotinamide adenine dinucleotide concentrations and redox balances of Xanthobacter flavus. J Bacteriol 182:4637–4639

    Article  CAS  Google Scholar 

  • Wang Y, Spalding MH (2006) An inorganic carbon transport system responsible for acclimation specific to air levels of CO2 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:10110–10115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Spalding MH (2014) LCIB in the Chlamydomonas CO2-concentrating mechanism. Photosynth Res 121:185–192

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Dunamu D, Spalding MH (2011) Carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii: inorganic carbon transport and CO2 recapture. Photosynth Res 109:115–122

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Stessman DJ, Spalding MH (2015) The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: how Chlamydomonas works against the gradient. Plant J. 82:429–448

    Article  PubMed  CAS  Google Scholar 

  • Winck FV, Arvidsson S, Riaño-Pachón DM, Hempel S, Koseska A, Nikoloski Z, Gomez DAU, Rupprecht J, Mueller-Roeber B (2013) Genome-wide identification of regulatory elements and reconstruction of gene regulatory networks of the green alga Chlamydomonas reinhardtii under carbon deprivation. PLoS One 8(11):e79909

    Article  CAS  PubMed  Google Scholar 

  • Woodger FJ, Bryant DA, 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang Y, Zhang J, Weeks DP (2001) The Cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii. Proc Natl Acad Sci 98:5341–5346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yamano T, Miura K, Fukuzawa H (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 147:340–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamano T, Tsujikawa T, Hatano K, Ozawa S, Takahashi Y, Fukuzawa H (2010) Light and low-CO2-dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol 51:1453–1468

    Article  CAS  PubMed  Google Scholar 

  • Yamano T, Sato E, Iguchi H, Fukuda Y, Fukuzawa H (2015) Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci 112:7315–7320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamauchi Y, Sugimoto Y (2010) Effect of protein modification by malondialdehyde on the interaction between the oxygen-evolving complex 33 kDa protein and photosystem II core proteins. Planta 231:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi Y, Kaniya Y, Kaneko Y, Hihara Y (2011) Physiological roles of the cyAbrB transcriptional regulator pair Sll0822 and Sll0359 in Synechocystis sp. strain PCC 6803. J Bacteriol 193:3702–3709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshizawa Y, Toyoda K, Arai H, Ishii M, Igarashi Y (2004) CO2-responsive expression and gene organization of three ribulose-1,5-bisphosphate carboxylase/oxygenase enzymes and carboxysomes in Hydrogenovibrio marinus strain MH-110. J Bacteriol 186:5685–5691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322:1110–1112

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Birla Institute of Technology and Sciences, Pilani, Rajasthan, India for providing infrastructural and logistic support. VT is thankful to DST-inspire fellowship program of Department of Science and Technology, India. GKS and PN thank UGC-BSR and CSIR, respectively, for their fellowships. This work was supported by SERB project EMR/2016/002470 sanctioned by the government of India to SM.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Birla Institute of Technology and Science, Pilani, 333031, Rajasthan, India

    Vandana Tomar, Gurpreet Kaur Sidhu, Panchsheela Nogia, Rajesh Mehrotra & Sandhya Mehrotra

Authors
  1. Vandana Tomar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gurpreet Kaur Sidhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Panchsheela Nogia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rajesh Mehrotra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sandhya Mehrotra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandhya Mehrotra.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Neal Stewart.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 15 kb)

Supplementary material 2 (DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomar, V., Sidhu, G.K., Nogia, P. et al. Regulatory components of carbon concentrating mechanisms in aquatic unicellular photosynthetic organisms. Plant Cell Rep 36, 1671–1688 (2017). https://doi.org/10.1007/s00299-017-2191-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2191-3

Keywords

Search

Navigation