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Uptake and utilization of inorganic carbon by cyanobacteria

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Molecular Biology of Photosynthesis
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Abstract

In the cyanobacteria, mechanisms exist that allow photosynthetic CO2 reduction to proceed efficiently even at very low levels of inorganic carbon. These inducible, active transport mechanisms enable the cyanobacteria to accumulate large internal concentrations of inorganic carbon that may be up to 1000-fold higher than the external concentration. As a result, the external concentration of inorganic carbon required to saturate cyanobacterial photosynthesis in vivo is orders of magnitude lower than that required to saturate the principal enzyme (ribulose bisphosphate carboxylase) involved in the fixation reactions. Since CO2 is the substrate for carbon fixation, the cyanobacteria somehow perform the neat trick of concentrating this small, membrane permeable molecule at the site of CO2 fixation. In this review, we will describe the biochemical and physiological experiments that have outlined the phenomenon of inorganic carbon accumulation, relate more recent genetic and molecular biological observations that attempt to define the constituents involved in this process, and discuss a speculative theory that suggests a unified view of inorganic carbon utilization by the cyanobacteria.

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Abbreviations

Ci :

Inorganic carbon

H-cells:

Cells grown under high CO2

L-cells:

Cells grown under low CO2

RuBP:

Ribulose-1,5-bisphosphate

WT:

Wild type

References

  • Abe T, Tsuzuki M and Miyachi S (1987) Transport and fixation of inorganic carbon during photosynthesis in cells of Anabaena grown under ordinary air III. Some characteristics of the HCO(stack) transport system in cells grown under ordinary air. Plant Cell Physiol 28: 867–874

    CAS  Google Scholar 

  • Aizawa K and Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Rev 39: 215–233

    Article  CAS  Google Scholar 

  • Andrews TJ and Abel KM (1981) Kinetics and subunit interactions of ribulose bisphosphate carboxylase-oxygenase from the cyanobacterium, Synechococcus sp. J Biol Chem 256: 8445–8451

    PubMed  CAS  Google Scholar 

  • Andrews TJ, Abel KM, Menzel E and Badger MR (1981) Molecular weight and quaternary structure of ribulose bisphosphate carboxylase from the cyanobacterium, Synehococcus sp. Arch Microbiol 130: 344–348

    Article  CAS  Google Scholar 

  • Badger MR (1980) Kinetic properties of RuBP carboxylase from Anabaena variabilis. Arch Biochem Biophys 201: 247–254

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Bassett M and Comins HN (1985) A model for HCO -3 accumulation and photosynthesis in the cyanobacterium Synechoccus sp. Plant Physiol 77: 465–471

    Article  PubMed  CAS  Google Scholar 

  • Bergman B, Codd GA and Hällbom L (1984) Glycollate excretion by N2-fixing cyanobacteria treated with photorespiratory inhibitors. Z Pflanzenphysiol 113: 451–460

    CAS  Google Scholar 

  • Bergman B, Codd GA, Hällbom L and Codd GA (1985) Effects of amino-oxyacetate and aminoacetonitrile on glycolate and ammonia release by the cyanobacterium Anabaena cylindrica. Plant Physiol 77: 536–539

    Article  PubMed  CAS  Google Scholar 

  • Codd GA and Marsden WJN (1984) The carboxysomes (polyhedral bodies) of autotrophic prokaryotes. Biol Rev 59: 389–422

    Article  CAS  Google Scholar 

  • Codd GA and Sallal A-KJ (1978) Glycolate oxidation by thylakoids of the cyanobacteria Anabaena cylindrica, Nostoc muscorum, and Chlorogloea fritschii. Planta 139: 177–181

    Article  CAS  Google Scholar 

  • Codd GA and Stewart WDP (1973) Pathways of glycollate metabolism in the blue—green alga Anabaena cylindrica. Arch Microbiol 124: 149–154

    Article  Google Scholar 

  • Codd GA and Stewart WDP (1976) Polyhedral bodies and ribulose 1,5-diphosphate carboxylase of the blue-green alga Anabaena cylindrica. Planta 130: 323–326

    Article  CAS  Google Scholar 

  • Coleman JR, Seeman JR and Berry JA (1982) RuBP carboxylase in carboxysomes of blue-green algae. Carnegie Inst of Wash Ybk 81: 83–87

    Google Scholar 

  • Colman B, Cheng K-H and Ingle RK (1976) The relative activities of PEP carboxylase and RuDP carboxylase in the blue-green algae. Plant Science Letters 6: 123–127

    Article  CAS  Google Scholar 

  • Creach E, Codd GA and Stewart WDP (1981) Primary products of photosynthesis and studies of carboxylating enzymes in the filamentous cyanobacterium Anabaena cylindrica. In: G. Akoyunoglou (ed.) Photosynthesis IV. Regulation of Carbon Metabolism, pp 49–56. Balaban International Science Services, Philadelphia, USA

    Google Scholar 

  • Espie GS and Canvin DT (1987) Evidence for Na+-independent HCO- 3 uptake by the cyanobacteriuim Synechococcus leopoliensis. Plant Physiol 84: 125–130

    Article  PubMed  CAS  Google Scholar 

  • Gatenby AA, van der Vies S and Bradley D (1985) Assembly in E. coli of a functional multisubunit ribulose bisphosphate carboxylase from a blue green alga. Nature 314: 617–620

    Article  CAS  Google Scholar 

  • Hawthornthwaite AM, Lanaras T and Codd GA (1985) Imuno-electronmicroscopic localization of Calvin cycle enzymes in Chlorogloeopsis fritschii. J Gen Microbiol 131: 2497–2500

    CAS  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 

  • Jordan DB and Ogren WL (1983) Species variation in the kinetic properties of ribulose 1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys 227: 425–433

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A (1985) Adaptation to low CO2 levels: Induction and the mechanism for inorganic carbon uptake. In: Lucas WJ and Berry JA (eds) Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, pp 325–328. Waverly Press/American Society of Plant Physiologists

    Google Scholar 

  • Kaplan A, Badger MR and Berry JA (1980) Photosynthesis and the intracellular inorganic carbon pool in the bluegreen alga Anabaena variabilis: Response to external CO2 concentration. Planta 149: 219–226

    Article  CAS  Google Scholar 

  • Kaplan A, Volokita M, Zenvirth D and Reinhold L (1984) An essential role for sodium in the bicarbonate transporting system of the cyanobacterium Anabaena variabilis. FEBS Lett 176: 166–168

    Article  CAS  Google Scholar 

  • Kaplan A, Zenvirth D, Marcus Y, Omata T and Ogawa T (1987) Energization and activation of inorganic carbon uptake by light in cyanobacteria. Plant Physiol 84: 210–213

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Zenvirth D, Reinhold L and Berry JA (1982) Involvement of a primary electrogenic pump in the mechanism for HCO- 3 uptake by the cyanobacterium Anabaena variabilis. Plant Physiol 69: 978–982

    Article  PubMed  CAS  Google Scholar 

  • Lanaras T, Hawthornthwaite AM and Codd GA (1985) Localization of carbonic anhydrase in the cyanobacterium Chlorogloeopsis fritschii. FEMS Microb Lett 26: 285–288

    Article  CAS  Google Scholar 

  • Lucas WJ and Berry JA (1985) Inorganic carbon uptake by aquatic photosynthetic organisms. Waverly Press, Baltimore, pp 1–480

    Google Scholar 

  • Marcus Y, Harel E and Kaplan A (1983) Adaptation of the cyanobacterium Anabaena variabilis to low CO2 concentration in their environment. Plant Physiol 71: 208–210

    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 

  • Marcus Y, Zenvirth D, Harel E and Kaplan A (1982) Induction of HCO -3 transporting capability and high photosynthetic affinity to inorganic carbon by low concentration of CO2 in Anabaena variabilis. Plant Physiol 69: 1008–1012

    Article  PubMed  CAS  Google Scholar 

  • Miller AG and Canvin DT (1985) Distinction between HCO -3 and CO2-dependent photosynthesis in the cyanobacterium Synechococcus leopoliensis based on the selective response of HCO -3 transport to Na+. FEBS Lett 187: 29–32

    Article  CAS  Google Scholar 

  • Miller AG and Canvin DT (1987) Na+-stimulation of photosynthesis in the cyanobacterium Synechococcus UTEX 625 grown on high levels of inorganic carbon. Plant Physiol 84: 118–124

    Article  PubMed  CAS  Google Scholar 

  • Miller AG and Colman B (1980) Active transport and accumulation of bicarbonate by a unicellular cyanobacterium. J Bacteriol 143: 1253–1259

    PubMed  CAS  Google Scholar 

  • Ogawa T and Kaplan A (1987) The stoichiometry between CO2 and H+ fluxes involved in the transport of inorganic carbon in cyanobacteria. Plant Physiol 83: 888–891

    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, Kaneda T and Omata T (1987) A mutant of Synechococcus PCC 7942 incapable of adapting to low CO2 concentration. Plant Physiol 84: 711–715

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Omata T and Ogawa T (1985) Changes in the polypeptide composition of the cytoplasmic membrane in 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 concentration. Plant Physiol 80: 525–530

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Ogawa T, Marcus Y, Friedberg D and Kaplan A (1987) Adaptation to low CO2 levels in a mutant of Anacystis nidulans R2 which requires high CO2 for growth. Plant Physiol 83: 892–894

    Article  PubMed  CAS  Google Scholar 

  • Pierce J, Carlson TJ and Williams JGK (1988) Anomalous oxygen sensitivity in a cyanobacterial mutant requiring the expression of ribulose bisphosphate carboxylase from a photosynthetic anaerobe. Submitted to Proc Nat Acad Sci

    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 

  • Reinhold L, Zviman M and Kaplan A (1987) Inorganic carbon fluxes and photosynthesis in cyanobacteria — a quantitative model. In: Biggins J (ed.) Progess in Photosynthesis Research, Vol 4, pp 289–296. Dordrecht: Martinus Nijhoff

    Google Scholar 

  • Shinozaki K and Sugiura M (1985) Genes for the large and small subunit of ribulose bisphosphate carboxylase/oxygenase constitute a single operon in a cyanobacterium Anacystis nidulans. 6301. Mol Gen Genet 200: 27–32

    Article  CAS  Google Scholar 

  • Spalding MH, Spreitzer RJ and Ogren WL (1983) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardtii. Planta 159: 261–266

    Article  CAS  Google Scholar 

  • Tabita FR and Small CL (1985) Expression and assembly of active cyanobacterial ribulose-1,5-bisphosphate carboxylase/oxygenase in Escherichia coli containing stoichiometric amounts of large and small subunits. Proc Nat Acad Sci USA 82: 6100–6103

    Article  PubMed  CAS  Google Scholar 

  • Takabe T, Nishimura M and Akazawa T (1976) Presence of two subunit types in ribulose 1,5-bisphosphate carboxylase from blue-green algae. Bioch Biophys Res Commun 68: 537–544

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yagawa Y, Shiraiwa Y and Miyachi S (1984) Carbonic anhydrase from the blue-green alga (cyanobacterium) Anabaena variabilis. Plant and Cell Physiol 25: 775–783

    CAS  Google Scholar 

  • Zenvirth D and Kaplan A (1981) Uptake and efflux of inorganic carbon in Dunaliella salina. Planta 152: 8–12

    Article  CAS  Google Scholar 

  • Zenvirth D, Volokita M and Kaplan A (1984) Evidence against H+-HCO -3 symport as the mechanism for HCO- 3 transport in the cyanobacterium Anabaena variabilis. J Membrane Biol 79: 271–274

    Article  CAS  Google Scholar 

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© 1988 Kluwer Academic Publishers

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Pierce, J., Omata, T. (1988). Uptake and utilization of inorganic carbon by cyanobacteria. In: Govindjee (eds) Molecular Biology of Photosynthesis. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-2269-3_28

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  • DOI: https://doi.org/10.1007/978-94-009-2269-3_28

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-7517-6

  • Online ISBN: 978-94-009-2269-3

  • eBook Packages: Springer Book Archive

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