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The dc13 gene upstream of ictB is involved in rapid induction of the high affinity Na+ dependent HCO3 − transporter in cyanobacteria

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Abstract

The phenomenon of rapid induction of high affinity HCO3 − uptake was investigated in two cyanobacterial species, Synechococcus strain PCC 7942 and Synechocystis strain PCC 6803. For both strains, mass spectrometric analysis of HCO3 − fluxes during steady state photosynthesis revealed that the high affinity HCO3 − uptake system was rapidly induced only in the presence of Na+. In Synechococcus there was a correlation between the capability of rapid induction of the high affinity HCO3 − uptake system and the appearance of the IctB protein. Neither fast induction of the high affinity HCO3 − uptake system nor IctB accumulation were prevented by chloramphenicol but by K252a. Inactivation of the gene dc13 upstream of ictB in Synechococcus led to the inability of the cells to rapidly induce the high affinity Na+ dependent HCO3 − uptake system although IctB was accumulated. The dc13 mutant was able to acclimate from high CO2 to 100 ppm CO2 by lowering the CO2 concentration step by step, while immediate decrease of the CO2 concentration to 100 ppm CO2 severely inhibited HCO3 − uptake. In Synechocystis the rapid induction of the Na+ dependent high affinity HCO3 − uptake system was not accompanied by an increase in sbtA RNA abundance, indicating that transcriptional regulation of sbtA is not responsible for the fast increase in substrate affinity of the HCO3 − transporter. The results are discussed in terms of post-translational modification of constitutively expressed components (e.g., SbtA)

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References

  • Amoroso G, Sültemeyer D, Thyssen C, Fock HP (1998) Uptake of HCO3¯ and CO2 in cells and chloroplasts from the micro algae Chlamydomonas reinhardtii and Dunaliella tertiolecta. Plant Physiol 116: 193–201

    Article  CAS  Google Scholar 

  • Badger MR, Palmqvist K, Yu JW (1994) Measurement of CO2 and HCO3¯ fluxes in cyanobacteria and microalgae during steadystate photosynthesis. Physiol Plant 90: 529–536

    Article  CAS  Google Scholar 

  • Bloye SA, Silman NJ, Mann NH, Carr, NG (1992) Bicarbonate concentration by Synechocystis PCC 6803: Modulation of protein phosphorylation and inorganic carbon transport by glucose. Plant Physiol 99: 601–606

    PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgramm quantities of protein utilizing the prinziple of protein-dye binding. Anal Biochem 72: 248–254

    Article  PubMed  CAS  Google Scholar 

  • Bonfil DJ, Ronen-Tarazi M, Sültemeyer D, Lieman-Hurwitz J, Schatz D, Kaplan A (1998) A putative HCO3¯ transporter in the cyanobacterium Synechococcus sp. strain PCC 7942. FEBS Lett 430: 236–240

    Article  PubMed  CAS  Google Scholar 

  • Figge RM, Cassier-Chauvat C, Chauvat F, Cerff R (2001) Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. Mol Microbiol 39: 455–468

    Article  PubMed  CAS  Google Scholar 

  • Fock HP, Sültemeyer DF (1989) O2 evolution and uptake measurements in plant cells by mass spectrometer. In Liskens HF and Jackson JF (eds) Modern Methods of Plant Analysis, Vol 9: 9–18. Springer-Verlag, Heidelberg, Germany

    Google Scholar 

  • Forchhammer K, Tandeau de Marsac N (1995) Functional analysis of the phosphoprotein PII (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 177: 2033–2044

    PubMed  CAS  Google Scholar 

  • Hisbergues M, Jeanjean R, Joset F, Tandeau de Marsac N, Bédu S (1999) Protein PII regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett 463: 216–220

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Reinhold L (1999) The CO2 concentrating mechanism in photosynthetic microorganisms. Ann Rev Plant Physiol Plant Mol Biol 50: 539–570

    Article  CAS  Google Scholar 

  • Klughammer B, Sültemeyer D, Badger MR, Price GD (1999) Involvement of NAD(P)H dehydrogenase subunits, NdhD3 and HdhF3, in high affinity CO2 uptake in Synechococcus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol Microbiol 32: 1305–1315

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685

    Article  PubMed  CAS  Google Scholar 

  • Maeda SH, 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

    Article  PubMed  CAS  Google Scholar 

  • Mann NH (1994) Protein phosphorylation in cyanobacteria. Microbiology 140: 3207–3215

    Article  PubMed  CAS  Google Scholar 

  • McKay RML, Gibbs SP, Espie GS (1993) Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of Rubisco and the mode of inorganic carbon transport in cells of the cyanobacterium UTEX 625. Arch Microbiol 159: 21–29

    Article  CAS  Google Scholar 

  • Ogawa T, Amichay D, Gurevitz M (1994) Isolation and characterisation of the ccmM gene requiered by the cyanobacterium Synechocystis PCC6803 for inorganic carbon utilization. Photosynth Res 39: 183–190

    Article  CAS  Google Scholar 

  • Ohkawa H, Pakrasi HB, Ogawa T (2000a) Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC 6803. J Biol Chem 275: 31630–31634

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Price GD, Badger MR, Ogawa T (2000b) Mutation of ndh genes leads to inhibition of CO2 uptake rather than HCO3+ uptake in Synechocystis sp. strain PCC 6803. J Bacteriol 182: 2591–2596

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Sonoda M, Shibata M, Ogawa T (2001) Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183: 4938–4939

    Article  PubMed  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

    PubMed  CAS  Google Scholar 

  • Omata T, Price GD, Badger MR, Okamura M, Gotha S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. PNAS 96: 13571–13576

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Gotha S, Takahashi Y, Harano Y, Maeda S-I (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183: 1891–1898

    Article  PubMed  CAS  Google Scholar 

  • Omata T, Takahashi Y, Yamaguchi O, Nishimura T (2002) Structure, function and regulation of the cyanobacterial high-affinity bicarbonate transporter BCT1. Funct Plant Biol 29: 151–159

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficient and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384–394

    CAS  Google Scholar 

  • Price GD and Badger MR (1989) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC 7942 creates a high CO2-requiring phenotype. Plant Physiol 91: 505–513

    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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Salon C, Mir NA, Canvin DT (1996) Influx and efflux of inorganic carbon in Synechococcus UTEX 625 Plant Cell Environ 19: 247–259

    CAS  Google Scholar 

  • Satoh R, Himeno M, Wadano A (1997) Carboxysomal diffusion resistence to ribulose 1,5-bisphosphate and 3-phosphoglycerate in the cyanobacterium Synechococcus PCC7942. Plant Cell Physiol 38: 769–775

    CAS  Google Scholar 

  • Schwarz R, Reinhold L, Kaplan A (1995) Low activation state of ribulose1,5-bisphosphate carboxylase/oxygenase in carboxysome-defective Synechococcus mutants. Plant Physiol 108: 183–190

    PubMed  CAS  Google Scholar 

  • Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. PNAS 98: 11789–11794

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T (2002a) Genes essential for sodiumdependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277: 18658–18664

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Ohkawa H, Katoh H, Shimoyama M, Ogawa T (2002b) Two CO2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis PCC6803. Funct Plant Biol 29: 123–129

    Article  CAS  Google Scholar 

  • Smith KS, Ferry JG (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24: 335–366

    Article  PubMed  CAS  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35: 171–205

    PubMed  CAS  Google Scholar 

  • Sültemeyer D, Price GD, Yu J-W, Badger MR (1995) Characterisation of carbon dioxide and bicarbonate transport during steady-state photosynthesis in the marine cyanobacterium Synechococcus strain PCC 7002. Planta 197: 597–607

    Article  Google Scholar 

  • Sültemeyer D, Klughammer B, Ludwig M, Badger MR, Price GD (1997) Random insertional mutagenesis used in the generation of mutants of the marine cyanobacterium Synechococcus sp. strain PCC 7002 with an impaired CO2 concentrating mechanism. Aust J Plant Pysiol 24: 317–327

    Article  Google Scholar 

  • Sültemeyer D, Klughammer B, Badger MR, Price DG (1998a) Fast induction of high-affinity HCO3¯ transport in cyanobacteria. Plant Physiol 116: 183–192

    Article  Google Scholar 

  • Sültemeyer D, Klughammer B, Badger MR, Price GD (1998b) Protein phosphorylation and its possible involvement in the induction of the high-affinity CO2 concentrating mechanism in cyanobacteria. Can J Bot 76: 954–961

    Article  Google Scholar 

  • Yu JW, Price GD, Badger MR (1994) Characterisation of CO2 and HCO3¯ uptake during steady-state photosynthesis in the cyanobacterium Synechococcus strain PCC7942. Aust J Plant Physiol 21: 185–195

    CAS  Google Scholar 

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  1. Fachbereich Biologie, Universität Kaiserslautern, Postfach 3049, 67653, Kaiserslautern, Germany

    Gabriele Amoroso, Nina Seimetz & Dieter Sültemeyer

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  1. Gabriele Amoroso
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  2. Nina Seimetz
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  3. Dieter Sültemeyer
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Amoroso, G., Seimetz, N. & Sültemeyer, D. The dc13 gene upstream of ictB is involved in rapid induction of the high affinity Na+ dependent HCO3 − transporter in cyanobacteria. Photosynthesis Research 77, 127–138 (2003). https://doi.org/10.1023/A:1025873718682

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