Photosynthesis Research

, Volume 77, Issue 2–3, pp 173–181 | Cite as

External HCO3 dehydration maintained by acid zones in the plasma membrane is an important component of the photosynthetic carbon uptake in Ruppia cirrhosa

  • Frida HellblomEmail author
  • Lennart Axelsson


Ruppia cirrhosa, a temperate seagrass growing in brackish water, featured a high capacity for HCO3 utilisation, which could operate over a wide pH range (from 7.5 up to 9.5) with maintained efficiency. Tris buffer inhibited this means of HCO3 utilisation in a competitive manner, while addition of acetazolamide, an inhibitor of extracellular carbonic anhydrase activity, caused a 40–50% inhibition. A mechanism involving periplasmic carbonic anhydrase-catalysed HCO3 dehydration in acid zones, followed by a (probably diffusive) transport of the formed CO2 across the plasma membrane was thus, at least partly, responsible for the HCO3 utilisation. This mechanism, which comprises a CO2-concentrating mechanism (CCM) associated with the plasma membrane, is thus shown for the first time in an aquatic angiosperm. Additional mechanisms involved in the Tris-sensitive HCO3 utilisation could be direct HCO3 uptake (e.g., in an H+/HCO3symport) or (more likely) non-catalysed HCO3 dehydration in the acid zones. Based on these results, and on earlier investigations on Zostera marina, a general model for analysis of HCO3 utilisation mechanisms of seagrasses is suggested. In this model, three `systems' for HCO3 utilisation are defined which are characterised (and can to some extent be quantified) by their capability to operate at high pH in combination with their response to acetazolamide and Tris. Some consequences of the fact that HCO3 utilisation and osmoregulation probably depend on the same energy source (ATP via H+-ATPase in the plasma membrane) are discussed.

acid zones AZ buffer carbonic anhydrase CCM Ruppia cirrhosa seagrass 


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  1. Axelsson L and Beer S (2001) Carbon limitation. In: Rai LC and Gaur JP (eds) Algal Adaptation to Environmental Stresses. Physiological, Biochemical and Molecular Mechanisms, pp 21–43. Springer-Verlag, BerlinGoogle Scholar
  2. Axelsson L, Ryberg H and Beer S (1995) Two modes of bicarbonate acquisition in Ulva lactuca. Plant Cell Environ 18: 439–445CrossRefGoogle Scholar
  3. Axelsson L, Larsson C and Ryberg H (1999) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant Cell Environ 22: 969–978CrossRefGoogle Scholar
  4. Axelsson L, Mercado JM and Figueroa FL (2000) Utilization of HCO3¯ at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35: 53–59Google Scholar
  5. Beer S and Rehnberg J (1997) The acquisition of inorganic carbon by the seagrass Zostera marina. Aquat Bot 56: 277–283CrossRefGoogle Scholar
  6. Beer S, Israel A, Drechsler Z and Cohen Y (1990) Photosynthesis of Ulva fasciata. V. Evidence for an inorganic carbon concentrating system, and Ribulose-1.5-biphosphate carboxylase/oxygenase CO2 kinetics. Plant Physiol 94: 1542–1546PubMedGoogle Scholar
  7. Beer S, Björk M, Hellblom F and Axelsson L (2002) Inorganic carbon utilization in marine angiosperms (seagrasses). Funct Plant Biol 29: 349–354CrossRefGoogle Scholar
  8. Björk M, Weil A, Semesi S and Beer S (1997) Photosynthetic utilisation of inorganic carbon by seagrasses from Zanzibar, East Africa. Mar Biol 129: 363–366CrossRefGoogle Scholar
  9. Cook CM and Colman B (1987) Some characteristics of photosynthetic inorganic carbon uptake of a marine macrophytic red alga. Plant Cell Environ 10: 275–278Google Scholar
  10. Drechsler Z, Sharkia R, Cabantchik ZI and Beer S (1993) Bicarbonate uptake in the marine macroalgae Ulva sp. is inhibited by classical probes of anion-exchange by red blood cells. Planta 191: 34–40CrossRefGoogle Scholar
  11. Fernández JA, García Sánchez MJ and Felle HH (1999) Physiological evidence for a proton pump and sodium exclusion mechanisms at the plasma membrane of the marine angiosperm Zostera marina L. J Exp Bot 50: 1763–1768CrossRefGoogle Scholar
  12. Ferrier J (1980) Apparent bicarbonate uptake and possible plasmalemma proton efflux in Chara corallina. Plant Physiol 66: 1198–1199PubMedCrossRefGoogle Scholar
  13. Hellblom F and Björk M(1999) Photosynthetic responses in Zostera marina to decreasing salinity, inorganic carbon content and osmolality. Aquat Bot 65: 97–104CrossRefGoogle Scholar
  14. Hellblom F, Beer S, Björk M and Axelsson L (2001) A buffer sensitive inorganic carbon utilisation system in Zostera marina. Aquat Bot 69: 55–62CrossRefGoogle Scholar
  15. Hellblom F, Moulin P, Björk M and Axelsson L (2002) Buffer sensitive carbon acquisition systems in submerged angiosperms - examples from marine and brackish water habitat. In: Hellblom F, Mechanisms of inorganic carbon acquisition in marine angiosperms (seagrasses). PhD thesis, Dept of Botany, Stockholm UniversityGoogle Scholar
  16. Jagels R and Barnabas A (1989) Variation in leaf ultrastructure of Ruppia maritima L. along a salinity gradient. Aquat Bot 33: 207–221CrossRefGoogle Scholar
  17. James PL and Larkum AWD (1996) Photosynthetic Ci acquisition of Posidonia australis. Aquat Bot 55: 149–157CrossRefGoogle Scholar
  18. Johnson KS (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limnol Oceanogr 27: 849–855CrossRefGoogle Scholar
  19. Larsson C and Axelsson L (1999) Bicarbonate uptake and utilization in marine macroalgae. Eur J Phycol 34: 79–86CrossRefGoogle Scholar
  20. Larsson C, Axelsson L, Ryberg H and Beer S (1997) Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rock pool. Eur J Phycol 32: 49–54CrossRefGoogle Scholar
  21. Les DH, Cleland MA and Waycott M (1997) Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22: 443–463CrossRefGoogle Scholar
  22. Lucas WJ (1977) Analogue inhibition of the active HCO3¯ transport site in the characean plasma membrane. J Exp Bot 28: 1321–1336Google Scholar
  23. Lucas WJ (1983) Photosynthetic assimilation of exogenous HCO3¯ by aquatic plants. Annu Rev Plant Physiol 34: 71–104CrossRefGoogle Scholar
  24. Lucas WJ, Keifer DW and Sanders D (1983) Bicarbonate transport in Chara corallina: Evidence for cotransport of HCO3¯ with H+. J Membr Biol 73: 263–274CrossRefGoogle Scholar
  25. Mercado JM, Figuéroa FL, Niell FX and Axelsson L (1997) A new method for estimating external carbonic anhydrase activity in macroalgae. J Phycol 33: 999–1006CrossRefGoogle Scholar
  26. Moroney JV, Husic HD and Tolbert NE (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Planta 195: 210–216Google Scholar
  27. Pak J-Y, Fukuhara T and Nitta T (1995) Discrete subcellular localization of membrane-bound ATPase activity in marine angiosperms and marine algae. Planta 196: 15–22PubMedCrossRefGoogle Scholar
  28. Palmgren MG(1998) Proton gradients and plant growth: Role of the plasmamembrane H+-ATPase. Adv Bot Res 28: 1–70Google Scholar
  29. Prins HBA, Snel J FH, Zanstra PE and Helder RJ (1982) The mechanism of bicarbonate assimilation by the polar leaves of Potamogeton and Elodea. CO2 concentrations at the leaf surface. Plant Cell Environ 5: 207–214Google Scholar
  30. Price GD and Badger MR (1985) Photosynthetic utilization of bicarbonate in Chara corallina. Aus J Plant Physiol 12: 257–267CrossRefGoogle Scholar
  31. Price GD, Badger MR, Bassett ME and Whitecross MI (1985) Involvement of plasmalemmasomes and carbonic anhydrase in photosynthetic utilization of bicarbonate in Chara corallina. Aust J Plant Physiol 12: 241–56Google Scholar
  32. Pytkowicz RM, Atlas E and Culberson CH (1977) Oceanography and Marine Biology. Ann Rev 15: 11–45Google Scholar
  33. Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27: 85–209CrossRefGoogle Scholar
  34. Sand-Jensen K and Gordon DM (1984) Differential ability of marine and freshwater macrophytes to utilize HCO3¯ and CO2. Mar Biol 80: 247–253CrossRefGoogle Scholar
  35. Spence DHN and Maberly SC (1985) Occurrence and ecological importance of HCO3¯ use among aquatic higher plants. In: Lucas WJ and Berry J (eds) Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, pp 125–143. American Society of Plant Physiologists, Rockville, MarylandGoogle Scholar
  36. Walker NA, Smith FA and Cathers IR (1980) Bicarbonate assimilation by fresh-water charophytes and higher plants. I. Membrane transport of bicarbonate ions is not proven. J Membr Biol 57: 51–58CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Department of Natural SciencesSodertorn University CollegeHuddingeSweden
  2. 2.Kristineberg Marine Research StationFiskebäckskilSweden

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