Skip to main content
SpringerLink
Log in

Specific features of the system of carbonic anhydrases of alkaliphilic cyanobacteria

  • Reviews
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

This review brings together our recent data on carbonic anhydrases of representatives of alkaliphilic cyanobacteria inhabiting soda lakes, which are considered as the relicts of the ancient terrestrial microbiota. The modern information about cyanobacterial carbonic anhydrases is based mainly on the study of model strains, such as Synechocystis and Synechococcus. Our results are compared with literature data. The role of carbonic anhydrases in the assimilation of inorganic carbon by cyanobacteria of soda lakes is discussed in terms of evolution of the CO2-concentrating mechanism.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

CA:

carbonic anhydrase(s)

CCM:

CO2-concentrating mechanism

Ci :

inorganic carbon (CO2/HC ORF −3 open reading frame

References

  1. De Simone, G. and Supuran, C.T., (In)organic anions as carbonic anhydrase inhibitors, J. Inorg. Biochem., 2012, vol. 111, pp. 117–129.

    Article  PubMed  Google Scholar 

  2. Smith, K.S. and Ferry, J.G., Prokaryotic carbonic anhydrases, FEMS Microbiol. Rev., 2000, vol. 24, pp. 335–366.

    Article  PubMed  CAS  Google Scholar 

  3. Price, G.D., Badger, M.R., Woodger, F.J., and Long, B.M., Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants, J. Exp. Bot., 2008, vol. 59, pp. 1441–1461.

    Article  PubMed  CAS  Google Scholar 

  4. Moroney, J.V., Ma, Y., Frey, W.D., Fusilier, K.A., Pham, T.T., Simms, T.A., DiMario, R.J., Yang, J., and Mukherjee, B., The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles, Photosynth. Res., 2011, vol. 109, pp. 133–149.

    Article  PubMed  CAS  Google Scholar 

  5. Kupriyanova, E.V. and Pronina, N.A., Carbonic anhydrase: enzyme that has transformed the biosphere, Russ. J. Plant Physiol., 2011, vol. 58, pp. 197–209.

    Article  CAS  Google Scholar 

  6. Markelova, A.G., Sinetova, M.P., Kupriyanova, E.V., and Pronina, N.A., Distribution and functional role of carbonic anhydrase Cah3 associated with thylakoid membranes in the chloroplast and pyrenoid of Chlamydomonas reinhardtii, Russ. J. Plant Physiol., 2009, vol. 56, pp. 761–768.

    Article  CAS  Google Scholar 

  7. Price, G.D., Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism, Photosynth. Res., 2011, vol. 109, pp. 47–57.

    Article  PubMed  CAS  Google Scholar 

  8. Cannon, G.C., Heinhorst, S., and Kerfeld, C.A., Carboxysomal carbonic anhydrases: structure and role in microbial CO2 fixation, Biochim. Biophys. Acta, 2010, vol. 1804, pp. 382–392.

    Article  PubMed  CAS  Google Scholar 

  9. Badger, M.R., Price, G.D., Long, B.M., and Woodger, F.J., The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism, J. Exp. Bot., 2006, vol. 57, pp. 249–265.

    Article  PubMed  CAS  Google Scholar 

  10. Zavarzin, G.A., The formation of the biosphere, Vestn. Ross. Akad. Nauk, 2001, vol. 71, pp. 988–1001.

    CAS  Google Scholar 

  11. Pronina, N.A., CO2-concentrating mechanisms (CCM) in the evolution of the biosphere, Problemy rannei evolyutsii fotosinteza (Problems of Early Evolution of Photosynthesis), Gorlenko, V.M. and Rozhnov, S.V., Eds., Moscow: Inst. Paleontology, Ross. Akad. Nauk, 2011, pp. 189–216.

    Google Scholar 

  12. Giordano, M., Beardall, J., and Raven, J.A., CO2-Concentrating Mechanism in Algae: Mechanisms, Environmental Modulation, and Evolution, Annu. Rev. Plant Biol, 2005, vol. 56, pp. 99–131.

    Article  PubMed  CAS  Google Scholar 

  13. Gerasimenko, L.M., Mityushina, L.L., and Namsaraev, B.B., Microcoleus mats from alkaliphilic and halophilic communities, Microbiology (Moscow), 2003, vol. 72, pp. 71–79.

    Article  CAS  Google Scholar 

  14. Dubinin, A.V., Gerasimenko, L.M., and Zavarzin, G.A., Ecophysiology and species diversity of cyanobacteria in Magadi Lake, Mickrobiologiya, 1995, vol. 64, pp. 845–849.

    CAS  Google Scholar 

  15. Wilbur, K.M. and Anderson, N.G., Electrometric and colorimetric determination of carbonic anhydrase, J. Biol. Chem., 1948, vol. 176, pp. 147–154.

    PubMed  CAS  Google Scholar 

  16. Dudoladova, M.V., Kupriyanova, E.V., Markelova, A.G., Sinetova, M.P., Allakhverdiev, S.I., and Pronina, N.A., The thylakoid carbonic anhydrase associated with photosystem is the component of inorganic carbon accumulating system in cells of halo- and alkaliphilic cyanobacterium Rhabdoderma lineare, BBA Bioenergetics, 2007, vol. 1767, pp. 616–623.

    Article  PubMed  CAS  Google Scholar 

  17. Kupriyanova, E., Villarejo, A., Markelova, A., Gerasimenko, L., Zavarzin, G., Samuelsson, G., Los, D., and Pronina, N., Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes, Microbiology (SGM), 2007, vol. 153, pp. 1149–1156.

    Article  CAS  Google Scholar 

  18. Soltes-Rak, E., Mulligan, M.E., and Coleman, J.R., Identification and characterization of gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria, J. Bacteriol., 1997, vol. 179, pp. 769–774.

    PubMed  CAS  Google Scholar 

  19. So, A.K., van Spall, H.G.C., Coleman, J.R., and Espie, G.S., Catalytic exchange of 18O from 13C18O-labelled CO2 by wild type cells and ecaA, ecaB, and ccaA mutants of the cyanobacteria Synechococcus PCC7942 and Synechocystis PCC6803, Can. J. Bot., 1998, vol. 76, pp. 1153–1160.

    CAS  Google Scholar 

  20. Kupriyanova, E.V., Sinetova, M.A., Markelova, A.G., Allakhverdiev, S.I., Los, D.A., and Pronina, N.A., Extracellular β-class carbonic anhydrase of the alkaliphilic cyanobacterium Microcoleus chthonoplastes, J. Photochem. Photobiol. B, 2011, vol. 103, pp. 78–86.

    Article  PubMed  CAS  Google Scholar 

  21. Sinetova, M.A., Kupriyanova, E.V., Markelova, A.G., Allakhverdiev, S.I., and Pronina, N.A., Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii, Biochim. Biophys. Acta, 2012, vol. 1817, pp. 1248–1255.

    Article  PubMed  CAS  Google Scholar 

  22. Shutova, T., Kenneweg, H., Buchta, J., Nikitina, J., Terentyev, V., Chernyshov, S., Andersson, B., Allakhverdiev, S.I., Klimov, V.V., Dau, H., Junge, W., and Samuelsson, G., The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal, EMBO J., 2008, vol. 5, pp. 782–791.

    Article  Google Scholar 

  23. So, A.K. and Espie, G.S., Cloning, characterization and expression of carbonic anhydrase from the cyanobacterium Synechocystis PCC6803, Plant Mol. Biol., 1998, vol. 37, pp. 205–215.

    Article  PubMed  CAS  Google Scholar 

  24. Siegesmund, M.A., Johansen, J.R., Karsten, U., and Friedl, T., Coleofasciculus gen. nov. (cyanobacteria): morphological and molecular criteria for revision of the genus Microcoleus Gomont, J. Phycol., 2008, vol. 44, pp. 1572–1585.

    Article  Google Scholar 

  25. Bolhuis, H., Severin, I., Confurius-Guns, V., Wollenzien, U.I., and Stal, L.J., Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes, ISME J., 2010, vol. 4, pp. 121–130.

    Article  PubMed  CAS  Google Scholar 

  26. Alber, B.E. and Ferry, J.G., Characterization of heterologously produced carbonic anhydrase from Methanosarcina thermophila, J. Bacteriol., 1996, vol. 178, pp. 3270–3274.

    PubMed  CAS  Google Scholar 

  27. Peña, K.L., Castel, S.E., de Araujo, C., Espie, G.S., and Kimber, M.S., Structural basis of the oxidative activation of the carboxysomal γ-carbonic anhydrase, CcmM, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 2455–2460.

    Article  PubMed  Google Scholar 

  28. Mikhodyuk, O.S., Zavarzin, G.A., and Ivanovskii, R.N., Transport systems for carbonate in the extremely natronophilic cyanobacterium Euhalothece sp., Microbiology (Moscow), 2008, vol. 77, pp. 412–418.

    Article  CAS  Google Scholar 

  29. Pronina, N.A., The organization and physiological role of the CO2-CM in microalgal photosynthesis, Russ. J. Plant Physiol., 2000, vol. 47, pp. 706–714.

    CAS  Google Scholar 

  30. Sergeev, V.N., Gerasimenko, L.M., and Zavarzin, G.A., The proterozoic history and present state of cyanobacteria, Microbiology (Moscow), 2002, vol. 71, pp. 623–637.

    Article  CAS  Google Scholar 

  31. Raven, J.A., Cockell, C.S., and de la Rocha, C.L., The evolution of inorganic carbon concentrating mechanisms in photosynthesis, Phil. Trans. R. Soc. London: B. Biol. Sci., 2008, vol. 363, pp. 2641–2650.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow, 127276, Russia

    E. V. Kupriyanova, M. A. Sinetova, A. G. Markelova, D. A. Los & N. A. Pronina

  2. Department of Biological Sciences, Graduate School of Analytical Science and Technology, Chungnam National University, Daejeon, 305-764, Republic of Korea

    S. M. Cho & Y. -I. Park

Authors
  1. E. V. Kupriyanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Sinetova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. M. Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Y. -I. Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. G. Markelova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. A. Los
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. A. Pronina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. V. Kupriyanova.

Additional information

Original Russian Text © E.V. Kupriyanova, M.A. Sinetova, S.M. Cho, Y.-I. Park, A.G. Markelova, D.A. Los, N.A. Pronina, 2013, published in Fiziologiya Rastenii, 2013, Vol. 60, No. 4, pp. 491–498.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kupriyanova, E.V., Sinetova, M.A., Cho, S.M. et al. Specific features of the system of carbonic anhydrases of alkaliphilic cyanobacteria. Russ J Plant Physiol 60, 465–471 (2013). https://doi.org/10.1134/S1021443713040079

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443713040079

Keywords

Search

Navigation