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Regulation of the mechanism for HCO 3 use by the inorganic carbon level in Porphyra leucosticta Thur. in Le Jolis (Rhodophyta)

Abstract

The capacity for HCO 3 use by Porphyra leucosticta Thur. in Le Jolis grown at different concentrations of inorganic carbon (Ci) was investigated. The use of HCO 3 at alkaline pH by P. leucosticta was demonstrated by comparing the O2 evolution rates measured with the O2 evolution rates theoretically supported by the CO2 spontaneously formed from HCO 3 . Both external and internal carbonic anhydrase (CA; EC 4.2.1.1) were implied in HCO 3 use during photosynthesis because O2 evolution rates and the increasing pH during photosynthesis were inhibited in the presence of azetazolamide and ethoxyzolamide (inhibitors for external and total CA respectively). Both external and internal CA were regulated by the Ci level at which the algae were grown. A high Ci level produced a reduction in total CA activity and a low Ci level produced an increase in total CA activity. In contrast, external CA was increased at low Ci although it was not affected at high Ci. Parallel to the reduction in total CA activity at high Ci is a reduction in the affinity for Ci, as estimated from photosynthesis versus Ci curves, was found. However, there was no evident relationship between external CA activity and the capacity for HCO 3 use because the presence of external CA became redundant when P. leucosticta was cultivated at high Ci. Our results suggest that the system for HCO 3 use in P. leucosticta is composed of different elements that can be activated or inactivated separately. Two complementary hypotheses are postulated: (i) internal CA is an absolute requirement for a functioning Ci-accumulation mechanism; (ii) there is a CO2 transporter that works in association with external CA.

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Abbreviations

AZ:

azetazolamide

CA:

carbonic anhydrase

Chl a :

chlorophyll a

Ci :

inorganic carbon

EZ:

6-ethoxyzolamide

gp :

photosynthetic conductance

PQ′:

photosynthetic quotient

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  • Axelsson L (1988) Changes in pH as a measure of photosynthesis by marine macroalgae. Mar Biol 97: 287–294

    Article  Google Scholar 

  • Axelsson L, Uusitalo J (1988) Carbon acquisition strategies for marine macroalgae. I. Utilization of proton exchanges visualized during photosynthesis in a closed system. Mar Biol 97: 295–300

    Article  CAS  Google Scholar 

  • Axelsson L, Uusitalo J, Ryberg H (1991) Mechanisms for concentrating and storage of inorganic carbon in marine macroalgae In: García-Reina G, Pedersén M (eds) Seaweed cellular biotechnology. Universided de las Palmas de Gran Canaria, pp 185–198

  • Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45: 369–392

    Article  CAS  Google Scholar 

  • Björk M, Haglund K, Ramazanov Z, Pedersén M (1993) Inducible mechanisms for HCO 3 utilization and repression of photorespiration in protoplast and thalli of three species of Ulva (Chlorophyta). J Phycol 29: 166–173

    Article  Google Scholar 

  • Cook CM, Lanaras T, Colman B (1986) Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. J Exp Bot 37: 977–984

    Article  CAS  Google Scholar 

  • Figueroa FL, Aguilera J, Niell FX (1995) Red and blue light regulation of growth and photosynthetic metabolism in porphyra umbilicalist (Bangiales, Rhodophyta). Eur J Phycol 30: 11–18

    Article  Google Scholar 

  • García-Sánchez MJ, Fernández JA, Niell X (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194: 55–61

    Article  Google Scholar 

  • Giordano M, Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81: 534–539

    Article  Google Scholar 

  • Gutknecht J, Bisson MA, Tosteson FC (1977) Diffusion of carbon dioxide through lipid bilayer membranes. Effects of carbonic anhydrase, bicarbonate and unstirred layers. J Gen Physiol 69: 779–794

    PubMed  Article  CAS  Google Scholar 

  • Haglund K, Björk M, Ramazanov Z, García-Reina G, Pedersén M (1992a) Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187: 275–281

    Article  CAS  Google Scholar 

  • Haglund K, Ramazanov Z, Mtolera M, Pedersén M (1992b) Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L. and Laminaria saccharina (L.) Lamour. (Phaeophyta). Planta 188: 1–6

    Article  CAS  Google Scholar 

  • Holbrook GP, Berr S, Spencer WE, Reiskind JB, Davis JS, Bowes G (1988) Photosynthesis in marine macroalgae: evidence for carbon limitation. Can J Bot 66: 577–582

    CAS  Google Scholar 

  • Inskeep W, Bloom PR (1985) Extinction coefficients of Chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol 77: 483–485

    PubMed  Article  CAS  Google Scholar 

  • Johnson KS (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limnol Oceanogr 27: 849–855

    CAS  Google Scholar 

  • Johnston AM, Raven JA (1987) The C4-like characteristics of the intertidal macroalga Ascophyllum nodosum (L.) Le Jolis (Fucales, Phaephyta). Phycologia 26: 159–166

    CAS  Google Scholar 

  • Johnston AM, Raven JA (1990) Effects of culture in high CO2 on the photosynthetic physiology of Fucus serratus. Bryo phycol J 25: 75–82

    Article  Google Scholar 

  • Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae. Oecologia 92: 317–326

    Article  Google Scholar 

  • Jolliffe EA, Tregunna EB (1970) Studies on HCO 3 ion uptake during photosynthesis in benthic marine algae. Phycologia 9: 293–303

    CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 277: 680–685

    Article  Google Scholar 

  • Lucas WJ (1983) Photosynthetic assimilation of exogenous HCO 3 by aquatic plants. Annu Rev Plant Physiol 34: 71–104

    Article  CAS  Google Scholar 

  • Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26: 439–449

    Article  CAS  Google Scholar 

  • Muñoz J, Merret MJ (1988) Inorganic carbon uptake in a smallcelled eukaryotic microalga. In: Rogers D, Gallon J (eds) Biochemistry of the algae and cyanobacteria (Proc Phytochem Soc Europe, vol 28, abstr.). Oxford University Press, Oxford, p43

    Google Scholar 

  • Nelson EB, Celedella A, Tolbert NE (1969) Carbonic anhydrase levels in Chlamydomonas. Phytochemistry 8: 2305–2306

    Article  CAS  Google Scholar 

  • Palmqvist K, Ramazanov Z, Samuelsson G (1990) The role of extracellular carbonic anhydrase for accumulation of inorganic carbon in the green alga Chlamydomonas reinhardii. A comparison between wild-type and cell-wall-less mutant cells. Physiol Plant 80: 267–276

    Article  CAS  Google Scholar 

  • Palmqvist K, Yu J-W, Badger MR (1994) Carbonic anhydrase activity and inorganic carbon fluxes in lowand high-Ci cells of Chlamydomonas reinhardtii and Scenedesmus obliquas. Physiol Plant 90: 537–547

    Article  CAS  Google Scholar 

  • Ramazanov Z, Cárdenas J (1992) Inorganic carbon transport across cell compartments of the halotolerant alga Dunaliella salina Physiol Plant 85: 121–128

    Article  CAS  Google Scholar 

  • Raven JA, Johnston AM (1991) Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources, Limnol Oceanogr 36: 1701–1714

    CAS  Article  Google Scholar 

  • Reiskind JB, Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA 88: 2883–2887

    PubMed  Article  CAS  Google Scholar 

  • Riley JP, Chester R (1977) Introduction to marine chemistry. Academic Press London, New York

    Google Scholar 

  • Rintamaki EA, Keys AJ, Parry MA (1988) Comparison of the specific activity of ribulose-l,5-bis-phospate carboxylase/oxygenase from some C3 and C4 plants. Physiol Plant 74: 326–331

    Article  CAS  Google Scholar 

  • Sokal PR, Rohlf FJ (1981) Biometry: the principles and practice of statistics in biological research, 2nd edn. W.H. Freeman San Francisco

    Google Scholar 

  • Starr R, Zeikus JA (1987) UTEX: the culture collection of algae at the University of Texas at Austin. J Phycol 23 [Suppl]: 1–47

    Article  Google Scholar 

  • Sültemeyer D, Miller AG, Espie GS, Fock HP, Canvin DT (1989) Active CO2 transport by the green alga Chlamydomonas reinhardtii. Plant Physiol 89: 1213–1219

    PubMed  Article  Google Scholar 

  • Sültemeyer D, Schmidt C, Heinrich PF (1993) Carbonic anhydrase in higher plants and aquatic microorganisms. Physiol Plant 88: 179–190

    Article  Google Scholar 

  • Surif MB, Raven JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78: 97–105

    Article  Google Scholar 

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This work was financed by the Ministry of Education and Science of Spain (MESS). J.M. Mercado is supported by a grant from Mess.

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Mercado, J.M., Niell, F.X. & Figueroa, F.L. Regulation of the mechanism for HCO 3 use by the inorganic carbon level in Porphyra leucosticta Thur. in Le Jolis (Rhodophyta). Planta 201, 319–325 (1997). https://doi.org/10.1007/s004250050073

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  • DOI: https://doi.org/10.1007/s004250050073

Key words

  • Carbonic anhydrase
  • Inorganic carbon
  • Macroalga
  • pH
  • Photosynthesis
  • Porphyra