Skip to main content

Chloroplastic Carbonic Anhydrases

  • Chapter
Regulation of Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 11))

Summary

In biological systems the interconversion between CO2 and HCO−+H+ is catalyzed by carbonic anhydrases (CAs). They belong to three evolutionary unrelated gene families designated α-, β- and γ-CA1 with no significant sequence homologies between representatives of the different CA families. In the stroma of higher plant chloroplasts a β-CA is one of the most abundant proteins. Its specific function is unclear but it is generally assumed to facilitate diffusion of CO2 to the active site of Rubisco. In the green algae Chlamydomonas reinhardtii, another CA, of α-type, was recently discovered. It is located inside the thylakoid lumen and is required for growth of C. reinhardtii under low CO2 conditions (0.035% CO2 in air). This CA is suggested to catalyze the production of CO2 and H2O inside the acidic lumenal compartment from HCO− that is pumped into the lumen by an as yet unknown mechanism. The third and most recently identified chloroplast CA was identified in Arabidopsis thaliana. The function of this α-type CA is not known but it is located in the chloroplast stroma. No chloroplastic γ-CA has yet been reported.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 379.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alber BE and Ferry JG (1994) A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci USA 91: 6909–6913

    CAS  PubMed  Google Scholar 

  • Aliev DA, Guliev NM, Mamedov TG, and Tsuprun VL (1986) Physicochemical properties and quaternary structure of chick pea leaf carbonic anhydrase. Biokhimiya 51:1785–1794

    CAS  Google Scholar 

  • Atkins CA (1974) Occurrence and some properties of carbonic anhydrase from legume root nodules. Phytochem 13: 93–98

    Article  CAS  Google Scholar 

  • Atkins CA, Patterson BD and Graham D (1972) Plant carbonic anhydrases. Plant Physiol 50: 218–223

    CAS  Google Scholar 

  • Björkbacka H, Johansson IM, Skårfstad E and Forsman C (1997) The sulfhydryl groups of Cys 269 and Cys 272 are critical for the oligomeric state of chloroplast carbonic anhydrase from Pisum sativum. Biochemistry 36: 4287–4294

    PubMed  Google Scholar 

  • Broun G, Selegny E, Minn CT and Thomas D (1970) Facilitated transport of CO2 across a membrane bearing carbonic anhydrase. FEBS Lett 7: 223–226

    Article  CAS  PubMed  Google Scholar 

  • Conlan RS, Griffiths LA, Napier JA, Shewry PR, Mantell S, Ainsworth C (1995) Isolation and characterisation of cDNA clones representing the genes encoding the major tuber storage protein (dioscorin) of yam (Dioscorea cayenensis Lam.). Plant Mol Biol 28: 369–380

    Article  CAS  PubMed  Google Scholar 

  • Eriksson M, Karlsson J, Ramazanov Z, Gardeström P and Samuelsson G (1996) Discovery of an algal mitochondrial carbonic anhydrase: Molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 93: 12031–12034

    Article  CAS  PubMed  Google Scholar 

  • Guilloton MB, Korte JJ, Lamblin AF, Fuchs JA and Anderson PM (1992) Carbonic anhydrase in Escherichia coli A product of the cyn operon. J Biol Chem 267: 3731–3734

    CAS  PubMed  Google Scholar 

  • Hatch MD and Burnell JN (1990) Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. Plant Physiol 93: 825–828

    CAS  Google Scholar 

  • Hewett-Emmett D and Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the α-, β-and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5: 50–77

    CAS  PubMed  Google Scholar 

  • Hill EP (1986) Inhibition of carbonic anhydrase by plasma of dogs and rabbits. J Appl Physiol 60:191–197

    CAS  PubMed  Google Scholar 

  • Hiltonen T, Björkbacka H, Forsman C, Clarke AK and Samuelsson G (1998) Intracellular β-carbonic anhydrase in the unicellular green alga Coccomyxa. Plant Physiol 117:1341–1349

    Article  CAS  PubMed  Google Scholar 

  • Johansson IM and Forsman C (1993) Kinetic studies of pea carbonic anhydrase. Eur J Biochem 218: 439–446

    Article  CAS  PubMed  Google Scholar 

  • Kamo T, Shimogawara K, Fukuzawa H, Muto S and Miyachi S (1990) Subunit constitution of carbonic anhydrase from Chlamydomonas reinhardtii. Eur J Biochem 192: 557–562

    Article  CAS  PubMed  Google Scholar 

  • Karlsson J, Hiltonen, T, Husic HD, Ramazanov Z and Samuelsson G (1995) Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 109: 533–539

    Article  CAS  PubMed  Google Scholar 

  • Karlsson K, Clarke AK, Chen Z, Hugghins SY, Park Y-I, Husic D, Moroney JV and Samuelsson G (1998) A novel α-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2 EMBO J 17: 1208–1216

    Article  CAS  PubMed  Google Scholar 

  • Khalifah RG (1971) The carbon dioxide hydration activity of carbonic anhydrase. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 246: 2561–2573

    CAS  PubMed  Google Scholar 

  • Kimber MS and Pai EF (2000) The active site architecture of Pisum sativum β-carbonic anhydrase is a mirror image of that of α-carbonic anhydrases. EMBO J 19: 1407–1418

    Article  CAS  PubMed  Google Scholar 

  • Kisker C, Schindelin H, Alber BE, Ferry JG and Rees DC (1996) A left-handed β-helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila. EMBO J 15: 2323–2330

    CAS  PubMed  Google Scholar 

  • Komarova Y, Doman N and Shaposhnikov G (1982) Two forms of carbonic anhydrase from bean chloroplasts. Biokhimiya/ Biochemistry (English translation). 47: 1027–1034

    CAS  Google Scholar 

  • Kuchitsu K, Tsuzuki M and Miyachi S (1988) Characterization of the pyrenoid isolated from the unicellular green alga Chlamydomonas reinhardtii: Paniculate form of Rubisco protein. Protoplasma 144: 17–24

    Article  CAS  Google Scholar 

  • Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Theor 74: 1–20

    CAS  Google Scholar 

  • Longmuir IS, Forster RE and Woo C-Y (1966) Diffusion of carbon dioxide through thin layers of solution. Nature 209: 393–394

    CAS  Google Scholar 

  • Majeau N, Arnoldo M and Coleman, JR (1994) Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. Plant Mol Biol 25: 377–385

    Article  CAS  PubMed  Google Scholar 

  • Meldrum NU and Roughton FJW (1933) Carbonic anhydrase: Its preparation and properties. J Physiol 80: 113–142

    CAS  Google Scholar 

  • Moroney JV, Bartlett SG, and Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24: 141–154

    CAS  Google Scholar 

  • Newman JR and Raven JA (1993) Carbonic anhydrase in Ranunculus penicillatus spp. Pseudofluitans: Activity, location and implications for carbon assimilation. Plant Cell Environ 16:491–500

    CAS  Google Scholar 

  • Newman T, deBruijn FJ, Green P, Keegstra K, Kende H, McIntosh L, Ohlrogge J, Raikhel N, Somerville S, Thomashow M, Retzel E and Somerville C (1994) Genes galore: A summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106: 1241–1255

    Article  CAS  PubMed  Google Scholar 

  • Park Y-I, Karlsson J, Rojdestvenski I, Pronina N, Klimov V, Öquist G and Samuelsson G. (1999) The role of the novel Photosystem II-associated carbonic anhydrase in carbon concentrating mechanism (CCM) in Chlamydomonas reinhardtii. FEBS Lett 444: 102–105

    Article  CAS  PubMed  Google Scholar 

  • Price GD, Coleman JR and Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus. PCC7942. Plant Physiol 100: 784–793

    CAS  Google Scholar 

  • Price GD, Howitt SM, Harrison K and Badger MR (1993) Analysis of genomic DNA region from the cyanobacterium Synechococcus sp strain PCC7942 involved in carboxysome assembly and function. J Bacteriol 175: 2871–2879

    CAS  PubMed  Google Scholar 

  • Price GD, Caemmerer Sv, Evans JR, Yu J-W, Lloyd J, Oja V, Kell P, Harrison K, Gallagher A and Badger MR (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340

    Article  CAS  Google Scholar 

  • Pronina NA and Semenenko, VE (1990) Membrane-bound carbonic anhydrase takes part in CO2 concentration in algae cells. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol IV, pp 489–492. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Raven JA (1995) Photosynthetic and non-photosynthetic roles of scarbonic anhydrase in algae and cyanobacteria. Phycologia 34: 93–101

    Google Scholar 

  • Raven JA (1997) CO2 concentrating mechanisms: A direct role for thylakoid lumen acidification? Plant Cell Environ 20: 147–154.

    Article  CAS  Google Scholar 

  • Reed ML and Graham, D. (1981) Carbonic anhydrase in plants: distribution, properties and possible physiological roles. In: Reinholdt L, Harborne JB, and Swain T (eds) Progress in Phytochemistry, Vol 7, pp 47–94. Pergamon Press, Oxford

    Google Scholar 

  • Semenenko VE, Avramova S, Georgiev D and Pronina NA (1997) Comparative study of activity and localisation of carbonic anhydrase in cells of Chlorella and Scenedesmus. Sov Plant Physiol 24: 852–856

    Google Scholar 

  • Smith RG (1988) Inorganic carbon transport in biological systems. Comp Biochem Physiol 90B: 639–654

    CAS  Google Scholar 

  • Soltes-Rak E, Mulligan ME and Coleman JR (1997) Identification of a gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria. J Bacteriol 179: 769–774

    CAS  PubMed  Google Scholar 

  • Stadie WC and O’Brien H (1933) The catalysis of the hydration of carbon dioxide and dehydration of carbonic acid by the enzyme isolated from red blood cells. J Biochem 103: 521–529

    CAS  Google Scholar 

  • Stemler AJ (1997) The case for chloroplast thylakoid carbonic anhydrase. Physiol Plant 99: 348–353

    Article  CAS  Google Scholar 

  • Tashian RE (1989) The carbonic anhydrases: Widening perspectives on their evolution, expression and function. Bioessays 10: 186–192

    Article  CAS  PubMed  Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana The Arabidopsis Genome Initiative. Nature 408: 796–815

    Article  Google Scholar 

  • Vaklinova SG, Goushtina LM and Lazova GN (1982) Carboanhydrase activity in chloroplasts and chloroplast fragments. C R Acad Bulg Sci 35: 1721–1724

    CAS  Google Scholar 

  • Warburg O and Krippahl G (1960) Notwendigkeit der kohlensaure für die chinon und ferricyanid-reaktionen in grünen grana. Z Naturforsch 15: 367–369

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2001 Kluwer Academic Publishers

About this chapter

Cite this chapter

Samuelsson, G., Karlsson, J. (2001). Chloroplastic Carbonic Anhydrases. In: Aro, EM., Andersson, B. (eds) Regulation of Photosynthesis. Advances in Photosynthesis and Respiration, vol 11. Springer, Dordrecht. https://doi.org/10.1007/0-306-48148-0_18

Download citation

  • DOI: https://doi.org/10.1007/0-306-48148-0_18

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-6332-3

  • Online ISBN: 978-0-306-48148-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics