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 HCO3 - transport system in cells grown under ordinary air. Plant Cell Physiol 28: 867–874
Aizawa K and Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Rev 39: 215–233
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
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
Badger MR (1980) Kinetic properties of RuBP carboxylase from Anabaena variabilis. Arch Biochem Biophys 201: 247–254
Badger MR and Andrews TJ (1982) Photosynthesis and inorganic carbon usage by the marine cyanobacterium, Synechococcus sp. Plant Physiol 70: 517–523
Badger MR, Bassett M and Comins HN (1985) A model for HCO3 - accumulation and photosynthesis in the cyanobacterium Synechoccus sp. Plant Physiol 77: 465–471
Bergman B, Codd GA and Hällbom L (1984) Glycollate excretion by N2-fixing cyanobacteria treated with photorespiratory inhibitors. Z Pflanzenphysiol 113: 451–460
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
Codd GA and Marsden WJN (1984) The carboxysomes (polyhedral bodies) of autotrophic prokaryotes. Biol Rev 59: 389–422
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
Codd GA and Stewart WDP (1973) Pathways of glycollate metabolism in the blue—green alga Anabaena cylindrica. Arch Microbiol 124: 149–154
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
Coleman JR, Seeman JR and Berry JA (1982) RuBP carboxylase in carboxysomes of blue-green algae. Carnegie Inst of Wash Ybk 81: 83–87
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
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
Espie GS and Canvin DT (1987) Evidence for Na+-independent HCO3 - uptake by the cyanobacteriuim Synechococcus leopoliensis. Plant Physiol 84: 125–130
Gatenby AA, van derVies 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
Hawthornthwaite AM, Lanaras T and Codd GA (1985) Imuno-electronmicroscopic localization of Calvin cycle enzymes in Chlorogloeopsis fritschii. J Gen Microbiol 131: 2497–2500
Jordan DB and Ogren WL (1981) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291: 513–515
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
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
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
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
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
Kaplan A, Zenvirth D, Reinhold L and Berry JA (1982) Involvement of a primary electrogenic pump in the mechanism for HCO3 - uptake by the cyanobacterium Anabaena variabilis. Plant Physiol 69: 978–982
Lanaras T, Hawthornthwaite AM and Codd GA (1985) Localization of carbonic anhydrase in the cyanobacterium Chlorogloeopsis fritschii. FEMS Microb Lett 26: 285–288
Lucas WJ and Berry JA (1985) Inorganic carbon uptake by aquatic photosynthetic organisms. Waverly Press, Baltimore, pp 1–480
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
Marcus Y, Schwarz R, Friedberg D and Kaplan A (1986) High CO2 requiring mutant of Anacystis nidulans R2. Plant Physiol 82: 610–612
Marcus Y, Zenvirth D, Harel E and Kaplan A (1982) Induction of HCO3 - transporting capability and high photosynthetic affinity to inorganic carbon by low concentration of CO2 in Anabaena variabilis. Plant Physiol 69: 1008–1012
Miller AG and Canvin DT (1985) Distinction between HCO3 - and CO2-dependent photosynthesis in the cyanobacterium Synechococcus leopoliensis based on the selective response of HCO3 - transport to Na+. FEBS Lett 187: 29–32
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
Miller AG and Colman B (1980) Active transport and accumulation of bicarbonate by a unicellular cyanobacterium. J Bacteriol 143: 1253–1259
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
Ogawa T and Ogren WL (1987) Action spectra for accumulation of inorganic carbon in the cyanobacterium Anabaena variabilis. Photochem Photobiol 41: 583–587
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
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
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
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
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
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
Reinhold L, Volokita M, Zenvirth D and Kaplan A (1984) Is HCO3 - transport in Anabaena a Na+ symport? Plant Physiol 76: 1090–1092
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
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
Spalding MH, Spreitzer RJ and Ogren WL (1983) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardtii. Planta 159: 261–266
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
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
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
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
Zenvirth D and Kaplan A (1981) Uptake and efflux of inorganic carbon in Dunaliella salina. Planta 152: 8–12
Zenvirth D, Volokita M and Kaplan A (1984) Evidence against H+-HCO3 - symport as the mechanism for HCO3 - transport in the cyanobacterium Anabaena variabilis. J Membrane Biol 79: 271–274
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Pierce, J., Omata, T. Uptake and utilization of inorganic carbon by cyanobacteria. Photosynth Res 16, 141–154 (1988). https://doi.org/10.1007/BF00039490
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DOI: https://doi.org/10.1007/BF00039490