Photosynthetica

, Volume 55, Issue 1, pp 3–19 | Cite as

Carbonic anhydrase — a universal enzyme of the carbon-based life

Review
First Online:
Received:
Accepted:

Abstract

Carbonic anhydrase (CA) is a metalloenzyme that performs interconversion between CO2 and the bicarbonate ion (HCO3 −). CAs appear among all taxonomic groups of three domains of life. Wide spreading of CAs in nature is explained by the fact that carbon, which is the major constituent of the enzyme’s substrates, is a key element of life on the Earth. Despite the diversity of CAs, they all carry out the same reaction of CO2/HCO3 − interconversion. Thus, CA obviously represents a universal enzyme of the carbon-based life. Within the classification of CAs, here we proposed the existence of an extensive family of CA-related proteins (γCA-RPs)–the inactive forms of γ-CAs, which are widespread among the Archaea, Bacteria, and, to a lesser extent, in Eukarya. This review focuses on the history of CAs discovery and integrates the most recent data on their classification, catalytic mechanisms, and physiological roles at various organisms.

Additional key words

active site carbon metabolism convergent evolution distribution functional role inhibitor activator inorganic carbon concentration 

Abbreviations

CA

carbonic anhydrase

CAI

carbonic anhydrase inhibitor

CA-RP

carbonic anhydrase-related protein

CCM

CO2-concentrating mechanism

Ci

inorganic carbon compounds (CO2 + HCO3 –)

hCA

human carbonic anhydrase

PSR

proton shuttle residue

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alber B.E., Ferry J.G.: A carbonic anhydrase from the archaeon Methanosarcina thermophila. - P. Natl. Acad. Sci. USA 91: 6909–6913, 1994.CrossRefGoogle Scholar
  2. Alterio V., Di Fiore A., D’Ambrosio K. et al.: Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? - Chem. Rev. 112: 4421–4468, 2012.PubMedCrossRefGoogle Scholar
  3. Alterio V., Langella E., Viparelli F. et al.: Structural and inhibition insights into carbonic anhydrase CDCA1 from the marine diatom Thalassiosira weissflogii. - Biochimie 94: 1232–1241, 2012.PubMedCrossRefGoogle Scholar
  4. Amoroso G., Morell-Avrahov L., Mü ller D., et al.: The gene NCE103 (YNL036w) from Saccharomyces cerevisiae encodes a functional carbonic anhydrase and its transcription is regulated by the concentration of inorganic carbon in the medium. - Mol. Microbiol. 56: 549–558, 2005.PubMedCrossRefGoogle Scholar
  5. Andersson B., Nyman P.O., Strid L.: Amino acid sequence of human erythrocyte CA B. - Biochem. Bioph. Res. Co. 48: 670–677, 1972.CrossRefGoogle Scholar
  6. Aspatwar A., Tolvanen M.E., Ortutay C., Parkkila S.: Carbonic anhydrase related proteins: molecular biology and evolution.–In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 135–156. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  7. Atkins C.A., Patterson B.D., Graham D.: Plant carbonic anhydrases I. Distribution of types among species. - Plant Physiol. 50: 214–217, 1972.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Blank C.E., Sánchez-Baracaldo P.: Timing of morphological and ecological innovations in the cyanobacteria–a key to understanding the rise of atmospheric oxygen. - Geobiology 8: 1–23, 2010.PubMedCrossRefGoogle Scholar
  9. Boone C.D., Pinard M., McKenna R., Silverman D.: Catalytic mechanism of α-class carbonic anhydrases: CO2 hydration and proton transfer.–In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 31–52. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  10. Coleman J.R.: Carbonic anhydrase and its role in photosynthesis.–In: Leegood R.C., Sharkey T.D., von Caemmerer S. (ed.): Photosynthesis: Physiology and Metabolism. Pp. 353–367. Kluwer Academic Publishers, Dordrecht 2000.CrossRefGoogle Scholar
  11. Cot S.S., So A.K., Espie G.S.: A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. - J. Bacteriol. 190: 936–945, 2008.PubMedCrossRefGoogle Scholar
  12. Cox E.H., McLendon G.L., Morel F.M. et al.: The active site structure of Thalassiosira weissflogii carbonic anhydrase 1. - Biochemistry 39: 12128–12130, 2000.PubMedCrossRefGoogle Scholar
  13. de Araujo C., Arefeen D., Tadesse Y. et al.: Identification and characterization of a carboxysomal γ-carbonic anhydrase from the cyanobacterium Nostoc sp. PCC 7120. - Photosynth. Res. 121: 135–150, 2014.PubMedCrossRefGoogle Scholar
  14. De Simone G., Di Fiore A., Capasso C., Supuran C.T.: The zinc coordination pattern in the η-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. - Bioorg. Med. Chem. Lett. 25: 1385–1389, 2015.PubMedCrossRefGoogle Scholar
  15. Del Prete S., Vullo D., De Luca V. et al.: Biochemical characterization of the δ-carbonic anhydrase from the marine diatom Thalassiosira weissflogii, TweCA. - J. Enzyme Inhib. Med. Chem. 29: 906–911, 2014.PubMedCrossRefGoogle Scholar
  16. Del Prete S., Vullo D., Fisher G.M. et al.: Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum–The η-carbonic anhydrases. - Bioorg. Med. Chem. Lett. 24: 4389–4396, 2014.PubMedCrossRefGoogle Scholar
  17. Del Prete S., Vullo D., Scozzafava A. et al.: Cloning, characterization and anion inhibition study of the δ-class carbonic anhydrase (TweCA) from the marine diatom Thalassiosira weissflogii. - Bioorgan. Med. Chem. 22: 531–537, 2014.CrossRefGoogle Scholar
  18. Domsic J.F., Avvaru B.S., Kim C.U. et al.: Entrapment of carbon dioxide in the active site of carbonic anhydrase II.–J. Biol. Chem. 283: 30766–30771, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Edman P., Begg G.: A protein sequenator. - Eur. J. Biochem. 1: 80–91, 1967.PubMedCrossRefGoogle Scholar
  20. Elleuche S., Pöggeler S.: Carbonic anhydrases in fungi. - Microbiology 156: 23–29, 2010.PubMedCrossRefGoogle Scholar
  21. Everson R.G.: Carbonic anhydrase and CO2 fixation in isolated chloroplasts. - Phytochemistry 9: 25–32, 1970.CrossRefGoogle Scholar
  22. Fernández C., Díaz E., García J.L.: Insights on the regulation of the phenylacetate degradation pathway from Escherichia coli. - Environ. Microb. Rep. 6: 239–250, 2014..CrossRefGoogle Scholar
  23. Fernández P.A., Hurd C.L., Roleda M.Y.: Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. - J. Phycol. 50: 998–1008, 2014.PubMedCrossRefGoogle Scholar
  24. Ferry J.G.: The gamma class of carbonic anhydrases. - Biochim. Biophys. Acta 1804: 374–381, 2010.PubMedCrossRefGoogle Scholar
  25. Field C.B., Behrenfel, M.J., Randerson J.T., Falkowski P.: Primary production of the biosphere: integrating terrestrial and oceanic components. - Science 281: 237–240, 1998.PubMedCrossRefGoogle Scholar
  26. Fromm S., Senkler J., Zabaleta E. et al.: The carbonic anhydrase domain of plant mitochondrial complex I. - Physiol. Plantarum 157: 289–296, 2016.CrossRefGoogle Scholar
  27. Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 9–30. Springer Science + Business Media, Dordrecht 2014.Google Scholar
  28. Frost S.C.: Physiological functions of the alpha class of carbonic anhydrases. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 9–30. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  29. Fukuzawa H., Suzuki E., Komukai Y., Miyachi S.: A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC 7942.–P. Natl. Acad. Sci. USA 89: 4437–4441, 1992.CrossRefGoogle Scholar
  30. Giordano M., Beardall J., Raven J.A.: CO2 concentrating mechanism in algae: mechanisms, environmental modulation, and evolution. - Annu. Rev. Plant. Biol. 56: 99–131, 2005.PubMedCrossRefGoogle Scholar
  31. Henderson L.E., Henriksson D., Nyman P.O.: Amino acid sequence of human erythrocyte carbonic anhydrase C. - Biochem. Bioph. Res. Co. 52: 1388–1394, 1973.CrossRefGoogle Scholar
  32. Henry R.P.: Multiple roles of carbonic anhydrase in cellular transport and metabolism. - Annu. Rev. Physiol. 58: 523–538, 1996.PubMedCrossRefGoogle Scholar
  33. Hewett-Emmett D., Hopkins P.J., Tashian R.E., Czelusniak J.: Origins and molecular evolution of the carbonic anhydrase isozymes. - Ann. NY Acad. Sci. 429: 338–358, 1984.PubMedCrossRefGoogle Scholar
  34. Hewett-Emmett D., Tashian R.E.: Functional diversity, conservation and convergence in the evolution of the α-, β- and γ- carbonic anhydrase gene families. - Mol. Phylogenet. Evol. 5: 50–77, 1996.PubMedCrossRefGoogle Scholar
  35. Hopkinson B.M., Dupont C.L., MatsudaY.: The physiology and genetics of CO2 concentrating mechanisms in model diatoms. - Curr. Opin. Plant Biol. 31: 51–57, 2016.PubMedCrossRefGoogle Scholar
  36. Iverson T.M., Alber B.E., Kisker C. et al.: A closer look at the active site of γ-carbonic anhydrases: High resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. - Biochemistry 39: 9222–9231, 2000.PubMedCrossRefGoogle Scholar
  37. Jansson C., Northen T.: Calcifying cyanobacteria–the potential of biomineralization for carbon capture and storage. - Curr. Opin. Biotechnol. 21: 365–371, 2010.PubMedCrossRefGoogle Scholar
  38. Jeyakanthan J., Rangarajan S., Mridula P. et al.: Observation of a calcium-binding site in the γ-class carbonic anhydrase from Pyrococcus horikoshii. - Acta Crystallogr. D 64: 1012–1019, 2008.PubMedCrossRefGoogle Scholar
  39. Jungnick N., Ma Y., Mukherjee B. et al.: The carbon concentrating mechanism in Chlamydomonas reinhardtii: finding the missing pieces. - Photosynth. Res. 121: 159–173, 2014.PubMedCrossRefGoogle Scholar
  40. Kamo T., Shimogawara K., Fukuzawa H. et al.: Subunit constitution of carbonic anhydrase from Chlamydomonas reinhardtii. - Eur. J. Biochem. 192: 557–562, 1990.PubMedCrossRefGoogle Scholar
  41. Kaplan A., Badger M.R., Berry J. A. Photosynthesis and the intracellular inorganic carbon pool in the blue-green alga Anabaena variabilis response to external CO2 concentration.–Planta 149: 219–226, 1980.PubMedCrossRefGoogle Scholar
  42. Karrasch M., Bott M., Thauer R.K.: Carbonic anhydrase activity in acetate grown Methanosarcina barkeri. - Arch. Microbiol. 151: 137–142, 1989.CrossRefGoogle Scholar
  43. Keilin D., Mann T.: Activity of purified carbonic anhydrase. - Nature 153: 107–108, 1944.CrossRefGoogle Scholar
  44. Kern D.M.: The hydration of carbon dioxide. - J. Chem. Educ. 37: 14–23, 1960.CrossRefGoogle Scholar
  45. Khalifah R.G.: The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. - J. Biol. Chem. 246: 2561–2573, 1971.PubMedGoogle Scholar
  46. Kimber M.S.: Carboxysomal carbonic anhydrases. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 89–103. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  47. Klodmann J., Sunderhaus S., Nimtz M. et al.: Internal architecture of mitochondrial complex I from Arabidopsis thaliana.–Plant Cell 22: 797–810, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Konhauser K.: Deepening the early oxygen debate. - Nat. Geosci. 2: 241–242, 2009.CrossRefGoogle Scholar
  49. Koonin E.V., Dolja V.V.: Virus world as an evolutionary network of viruses and capsidless selfish elements. - Microbiol. Mol. Biol. Rev. 78: 278–303, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kozliak E.I., Guilloton M.B., Gerami-Nejad M. et al.: Expression of proteins encoded by the Escherichia coli cyn operon: carbon dioxide-enhanced degradation of carbonic anhydrase. - J. Bacteriol. 176: 5711–5717, 1994.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kumar R.S., Ferry J.G.: Prokaryotic carbonic anhydrases of Earth's environment. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 77–87. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  52. Kupriyanova E., Villarejo A., Markelova A. et al.: Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes.–Microbiology 153: 1149–1156, 2007.PubMedCrossRefGoogle Scholar
  53. Kupriyanova E.V, Pronina N.A.: Carbonic anhydrase: enzyme that has transformed the biosphere. - Russ. J. Plant Physl+ 58: 197–209, 2011.CrossRefGoogle Scholar
  54. Kupriyanova E.V., Sinetova M.A., Cho S.M. et al.: CO2- concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role and evolutionary origin. - Photosynth. Res. 117: 133–146, 2013.PubMedCrossRefGoogle Scholar
  55. 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. Physl+ 60: 465–471, 2013.CrossRefGoogle Scholar
  56. Kustka A.B., Milligan A.J., Zheng H.Y. et al.: Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana. - New Phytol. 204: 507–520, 2014.PubMedCrossRefGoogle Scholar
  57. Lane T.W., Morel F.M.: A biological function for cadmium in marine diatoms. - P. Natl. Acad. Sci. USA 97: 4627–4631, 2000.CrossRefGoogle Scholar
  58. Lane T.W., Saito M.A., George G.N. et al.: A cadmium enzyme from a marine diatom. - Nature 435: 42, 2005.PubMedCrossRefGoogle Scholar
  59. Larsson C., Axelsson L.: Bicarbonate uptake and utilization in marine macroalgae. - Eur. J. Phycol. 34: 79–86, 1999.CrossRefGoogle Scholar
  60. Liljas A., Kannan K.K., Bergstén P.C. et al.: Crystal structure of human carbonic anhydrase C. - Nature 235: 131–137, 1972.Google Scholar
  61. Liljas A., Laurberg M.: A wheel invented three times. The molecular structures of the three carbonic anhydrases. - EMBO Rep. 1: 16–17, 2000.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lin K.-T.D., Deutsch H.F.: Human carbonic anhydrase. XI. The complete primary structure of carbonic anhydrase B. - J. Biol. Chem. 248: 1885–1893, 1973.PubMedGoogle Scholar
  63. Lin K.-T.D., Deutsch H.F.: Human carbonic anhydrase. XII. The complete primary structure of carbonic anhydrase C. - J.Biol. Chem. 249: 2329–2337, 1974.PubMedGoogle Scholar
  64. Lindskog S.: Structure and mechanism of carbonic anhydrase. - Pharmacol. Therapeut. 74: 1–20, 1997.CrossRefGoogle Scholar
  65. Long B.M., Rae B.D., Rolland V. et al.: Cyanobacterial CO2- concentrating mechanism components: function and prospects for plant metabolic engineering. - Curr. Opin. Plant. Biol. 31: 1–8, 2016.PubMedCrossRefGoogle Scholar
  66. Ludwig M.: Evolution of carbonic anhydrase in C4 plants. - Curr. Opin. Plant Biol. 31: 16–22, 2016.PubMedCrossRefGoogle Scholar
  67. Markelova A.G., Sinetova M.P., Kupriyanova E.V., Pronina N.A.: Distribution and functional role of carbonic anhydrase Cah3 associated with thylakoid in chloroplast and pyrenoid of Chlamydomonas reinhardtii. - Russ. J. Plant. Physl+. 56: 761–768, 2009.CrossRefGoogle Scholar
  68. McKenna R., Supuran C.T.: Carbonic anhydrase inhibitors drug design.–In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 291–323. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  69. Meldrum N.N., Rounghton F.J.W.: Carbonic anhydrase: its preparation and properties. - J. Physiol. 80: 113–142, 1933.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Merlin C., Masters M., McAteer S., Coulson A.: Why is carbonic anhydrase essential to Escherichia coli? - J. Bacteriol. 185: 6415–6424, 2003.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mitsuhashi S., Mizushima T., Yamashita E. et al.: X-ray structure of β-carbonic anhydrase from the red alga, Porphyridium purpureum, reveals a novel catalytic site for CO2 hydration. - J. Biol. Chem. 275: 5521–5526, 2000.PubMedCrossRefGoogle Scholar
  72. Moroney J.V., Ma Y., Frey W.D. et al.: The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. - Photosynth. Res. 109Google Scholar
  73. Hewett-Emmett D., Tashian R.E.: Functional diversity, conservation and convergence in the evolution of the α-, β- and γ- carbonic anhydrase gene families.–Mol. Phylogenet. Evol. 5: 50–77, 1996.PubMedCrossRefGoogle Scholar
  74. Hopkinson B.M., Dupont C.L., MatsudaY.: The physiology and genetics of CO2 concentrating mechanisms in model diatoms. - Curr. Opin. Plant Biol. 31: 51–57, 2016.PubMedCrossRefGoogle Scholar
  75. Iverson T.M., Alber B.E., Kisker C. et al.: A closer look at the active site of γ-carbonic anhydrases: High resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. - Biochemistry 39: 9222–9231, 2000.PubMedCrossRefGoogle Scholar
  76. Jansson C., Northen T.: Calcifying cyanobacteria–the potential of biomineralization for carbon capture and storage. - Curr. Opin. Biotechnol. 21: 365–371, 2010.PubMedCrossRefGoogle Scholar
  77. Jeyakanthan J., Rangarajan S., Mridula P. et al.: Observation of a calcium-binding site in the γ-class carbonic anhydrase from Pyrococcus horikoshii. - Acta Crystallogr. D 64: 1012–1019, 2008.PubMedCrossRefGoogle Scholar
  78. Jungnick N., Ma Y., Mukherjee B. et al.: The carbon concentrating mechanism in Chlamydomonas reinhardtii: finding the missing pieces. - Photosynth. Res. 121: 159–173, 2014.PubMedCrossRefGoogle Scholar
  79. Kamo T., Shimogawara K., Fukuzawa H. et al.: Subunit constitution of carbonic anhydrase from Chlamydomonas reinhardtii. - Eur. J. Biochem. 192: 557–562, 1990.PubMedCrossRefGoogle Scholar
  80. Kaplan A., Badger M.R., Berry J.A. Photosynthesis and the intracellular inorganic carbon pool in the blue-green alga Anabaena variabilis response to external CO2 concentration.–Planta 149: 219–226, 1980.PubMedCrossRefGoogle Scholar
  81. Karrasch M., Bott M., Thauer R.K.: Carbonic anhydrase activity in acetate grown Methanosarcina barkeri. - Arch. Microbiol. 151: 137–142, 1989.CrossRefGoogle Scholar
  82. Keilin D., Mann T.: Activity of purified carbonic anhydrase. - Nature 153: 107–108, 1944.CrossRefGoogle Scholar
  83. Kern D.M.: The hydration of carbon dioxide. - J. Chem. Educ. 37: 14–23, 1960.CrossRefGoogle Scholar
  84. Khalifah R.G.: The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. - J. Biol. Chem. 246: 2561–2573, 1971.PubMedGoogle Scholar
  85. Kimber M.S.: Carboxysomal carbonic anhydrases. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 89–103. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  86. Klodmann J., Sunderhaus S., Nimtz M. et al.: Internal architecture of mitochondrial complex I from Arabidopsis thaliana.–Plant Cell 22: 797–810, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Konhauser K.: Deepening the early oxygen debate. - Nat. Geosci. 2: 241–242, 2009.CrossRefGoogle Scholar
  88. Koonin E.V., Dolja V.V.: Virus world as an evolutionary network of viruses and capsidless selfish elements. - Microbiol. Mol. Biol. Rev. 78: 278–303, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kozliak E.I., Guilloton M.B., Gerami-Nejad M. et al.: Expression of proteins encoded by the Escherichia coli cyn operon: carbon dioxide-enhanced degradation of carbonic anhydrase. - J. Bacteriol. 176: 5711–5717, 1994.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Kumar R.S., Ferry J.G.: Prokaryotic carbonic anhydrases of Earth's environment. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 77–87. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  91. Kupriyanova E., Villarejo A., Markelova A. et al.: Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes.–Microbiology 153: 1149–1156, 2007.PubMedCrossRefGoogle Scholar
  92. Kupriyanova E.V, Pronina N.A.: Carbonic anhydrase: enzyme that has transformed the biosphere. - Russ. J. Plant Physl+ 58: 197–209, 2011.CrossRefGoogle Scholar
  93. Kupriyanova E.V., Sinetova M.A., Cho S.M. et al.: CO2- concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role and evolutionary origin. - Photosynth. Res. 117: 133–146, 2013.PubMedCrossRefGoogle Scholar
  94. 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. Physl+ 60: 465–471, 2013.CrossRefGoogle Scholar
  95. Kustka A.B., Milligan A.J., Zheng H.Y. et al.: Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana. - New Phytol. 204: 507–520, 2014.PubMedCrossRefGoogle Scholar
  96. Lane T.W., Morel F.M.: A biological function for cadmium in marine diatoms. - P. Natl. Acad. Sci. USA 97: 4627–4631, 2000.CrossRefGoogle Scholar
  97. Lane T.W., Saito M.A., George G.N. et al.: A cadmium enzyme from a marine diatom. - Nature 435: 42, 2005.PubMedCrossRefGoogle Scholar
  98. Larsson C., Axelsson L.: Bicarbonate uptake and utilization in marine macroalgae. - Eur. J. Phycol. 34: 79–86, 1999.CrossRefGoogle Scholar
  99. Liljas A., Kannan K.K., Bergstén P.C. et al.: Crystal structure of human carbonic anhydrase C. - Nature 235: 131–137, 1972.Google Scholar
  100. Liljas A., Laurberg M.: A wheel invented three times. The molecular structures of the three carbonic anhydrases. - EMBO Rep. 1: 16–17, 2000.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Lin K.-T.D., Deutsch H.F.: Human carbonic anhydrase. XI. The complete primary structure of carbonic anhydrase B. - J. Biol. Chem. 248: 1885–1893, 1973.PubMedGoogle Scholar
  102. Lin K.-T.D., Deutsch H.F.: Human carbonic anhydrase. XII. The complete primary structure of carbonic anhydrase C. - J. Biol. Chem. 249: 2329–2337, 1974.PubMedGoogle Scholar
  103. Lindskog S.: Structure and mechanism of carbonic anhydrase. - Pharmacol. Therapeut. 74: 1–20, 1997.CrossRefGoogle Scholar
  104. Long B.M., Rae B.D., Rolland V. et al.: Cyanobacterial CO2- concentrating mechanism components: function and prospects for plant metabolic engineering. - Curr. Opin. Plant. Biol. 31: 1–8, 2016.PubMedCrossRefGoogle Scholar
  105. Ludwig M.: Evolution of carbonic anhydrase in C4 plants. - Curr. Opin. Plant Biol. 31: 16–22, 2016.PubMedCrossRefGoogle Scholar
  106. Markelova A.G., Sinetova M.P., Kupriyanova E.V., Pronina N.A.: Distribution and functional role of carbonic anhydrase Cah3 associated with thylakoid in chloroplast and pyrenoid of Chlamydomonas reinhardtii. - Russ. J. Plant. Physl+. 56: 761–768, 2009.CrossRefGoogle Scholar
  107. McKenna R., Supuran C.T.: Carbonic anhydrase inhibitors drug design. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 291–323. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  108. Meldrum N.N., Rounghton F.J.W.: Carbonic anhydrase: its preparation and properties.–J. Physiol. 80: 113–142, 1933.PubMedPubMedCentralCrossRefGoogle Scholar
  109. Merlin C., Masters M., McAteer S., Coulson A.: Why is carbonic anhydrase essential to Escherichia coli? - J. Bacteriol. 185: 6415–6424, 2003.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Mitsuhashi S., Mizushima T., Yamashita E. et al.: X-ray structure of β-carbonic anhydrase from the red alga, Porphyridium purpureum, reveals a novel catalytic site for CO2 hydration. - J. Biol. Chem. 275: 5521–5526, 2000.PubMedCrossRefGoogle Scholar
  111. Moroney J.V., Ma Y., Frey W.D. et al.: The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. - Photosynth. Res. 109: 133–149, 2011.PubMedCrossRefGoogle Scholar
  112. Nasir A., Kim K.M., Caetano-Anolles G.: Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya. - BMC Evol. Biol. 12: 156, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Neish A.C.: Studies on chloroplasts, their chemical composition and the distribution of certain metabolites between the chloroplasts and the remainder of the leaf. - Biochem. J. 33: 300–308, 1939.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Nichiporovich A.A.: [Light and carbon nutrition of plants–photosynthesis] Pp. 12. Publ. Academy of Sciences of the USSR, Moscow 1955. [In Russian]Google Scholar
  115. Parfrey L.W. Barbero E., Lasser E. et al.: Evaluating support for the current classification of eukaryotic diversity. - PLoS Genet. 2: e220, 2006.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Park H., Song B., Morel F.M.M.: Diversity of the cadmiumcontaining carbonic anhydrase in marine diatoms and natural waters.–Environ. Microbiol. 9: 403–413, 2007.PubMedCrossRefGoogle Scholar
  117. Park H.M., Park J.H., Choi J.W. et al.: Structures of the gammaclass carbonic anhydrase homologue YrdA suggest a possible allosteric switch. - Acta Crystallogr. 68: 920–926, 2012.Google Scholar
  118. Peãa K.L., Castel S.E., de Araujo C. et al.: Structural basis of the oxidative activation of the carboxysomal γ-carbonic anhydrase, CcmM. - P. Natl. Acad. Sci. USA 107: 2455–2460, 2010.CrossRefGoogle Scholar
  119. Price G.D., Badger M.R., Wodger F.J., 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. 59: 1441–1461, 2008.PubMedCrossRefGoogle Scholar
  120. Price G.D., Coleman, J.R., Badger M.R.: Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC 7942. - Plant Physiol. 100: 784–793, 1992.PubMedPubMedCentralCrossRefGoogle Scholar
  121. Price G.D., von Caemmerer S., Evans J.R. et al.: 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, 1994.CrossRefGoogle Scholar
  122. Price G.D.: Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. - Photosynth. Res. 109: 47–57, 2011.PubMedCrossRefGoogle Scholar
  123. Pronina N.A., Borodin V.V.: CO2 stress and CO2 concentration mechanism: investigation by means of photosystem-deficient and carbonic anhydrase-deficient mutants of Chlamydomonas reinhardtii. - Photosynthetica 28: 515–522, 1993.Google Scholar
  124. Rabinowitch E.I.: Photosynthesis and Related Processes. Pp. 177. Interscience Publishers, New York 1945.Google Scholar
  125. Rautenberger R., Fernández P.A., Strittmatter M. et al.: Saturating light and not increased carbon dioxide under ocean acidification drives photosynthesis and growth in Ulva rigida (Chlorophyta). - Ecol. Evol. 5: 874–888, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Raven J.A., Beardall J.: CO2 concentrating mechanisms and environmental change. - Aquat. Bot. 118: 24–37, 2014.CrossRefGoogle Scholar
  127. Raven J.A., Beardall J.: The ins and outs of CO2. - J. Exp. Bot. 67: 1–13, 2016.PubMedCrossRefGoogle Scholar
  128. Raven J.A., Hurd C.J.: Ecophysiology of photosynthesis in macroalgae. - Photosynth. Res. 113: 105–125, 2012.PubMedCrossRefGoogle Scholar
  129. Reungprapavut S., Krungkrai S.R., Krungkrai J.: Plasmodium falciparum carbonic anhydrase is a possible target for malaria chemotherapy. - J. Enzym. Inhib. Med. Ch. 19: 249–256, 2004.CrossRefGoogle Scholar
  130. Roberts S.B., Lane T.W., Morel F.M.: Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). - J. Phycol. 33: 845–850, 1997.CrossRefGoogle Scholar
  131. Rowlett R.S.: Structure and catalytic mechanism of β-carbonic anhydrases. - In: Frost S.C., McKenna R. (ed.): Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcell. Biochem. Pp. 53–76. Springer Science + Business Media, Dordrecht 2014.CrossRefGoogle Scholar
  132. Rudenko N.N., Ignatova L.K., Fedorchuk T.P., Ivanov B.N.: Carbonic anhydrases in photosynthetic cells of higher plants.–Biochemistry-Moscow+ 80: 674–687, 2015.PubMedCrossRefGoogle Scholar
  133. Sanger F., Niclein S., Coulson A.R.: DNA sequencing with chain-terminating inhibitors. - P. Natl. Acad. Sci. USA 74: 5463–5467, 1977.CrossRefGoogle Scholar
  134. Sawaya M.R., Cannon G.C., Heinhorst S. et al.: The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. - J. Biol. Chem. 17: 7546–7555, 2006.CrossRefGoogle Scholar
  135. Shutova T., Kenneweg H., Buchta J. et al.: The photosystem IIassociated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal. - EMBO J. 27: 782–791, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  136. Silverman D.N., Lindskog S.: The catalytic mechanism of carbonic anhydrase: implications of a rate-limiting proteolysis of water. - Acc. Chem. Res. 21: 30–36, 1988.CrossRefGoogle Scholar
  137. Silverman D.N., McKenna R.: Solvent-mediated proton transfer in catalysis by carbonic anhydrase. - Acc. Chem. Res. 40: 669–675, 2007.PubMedCrossRefGoogle Scholar
  138. Sinetova M.A., Kupriyanova E.V., Markelova A.G. et al.: Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii. - Biochim. Biophys. Acta 1817: 1248–1255, 2012.PubMedCrossRefGoogle Scholar
  139. Smith K.S., Ferry J.G.: Prokaryotic carbonic anhydrases. - FEMS Microbiol. Rev. 24: 335–366, 2000.PubMedCrossRefGoogle Scholar
  140. Smith K.S., Jakubzic C., Whitta T.S., Ferry J.G.: Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. - P. Natl. Acad. Sci. USA 96: 15184–15189, 1999.CrossRefGoogle Scholar
  141. Smith К.S., Ferry J.G.: А plant type (β-class) carbonic anhydrase from the thermophilic methanoarchaeon Methanobacterium thermoautotrophicum. - J. Bacteriol. 181: 6247–6253, 1999.PubMedPubMedCentralGoogle Scholar
  142. So A.K., Espie G.S., Williams E.B. et al.: A novel evolutionary lineage of carbonic anhydrase (epsilon class) is a component of the carboxysome shell. - J. Bacteriol. 186: 623–630, 2004.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Soltes-Rak E., Mulligan M.E., Coleman J.R.: Identification and characterization of gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria. - J. Bacteriol. 179: 769–774, 1997.PubMedPubMedCentralCrossRefGoogle Scholar
  144. Stadie W.C., O’Brien H.: The catalysis of the hydration of carbonic dioxide and dehydration of carbonic acid by the enzyme from red blood cells. - J. Biol. Chem. 103: 521–529, 1933.Google Scholar
  145. Suarez Covarrubias A., Larsson T.A., Hégbom M. et al.: Structure and function of carbonic anhydrases from Mycobacterium tuberculosis. - J. Biol. Chem. 280: 18782–18789, 2005.PubMedCrossRefGoogle Scholar
  146. Supuran C.T, Scozzafava A.: Carbonic anhydrases as targets for medicinal chemistry. - Bioorgan. Med. Chem. 15: 4336–4350, 2007.CrossRefGoogle Scholar
  147. Supuran C.T.: Carbonic anhydrases: catalytic and inhibition mechanisms, distribution and physiological roles. - In: Supuran C.T., Scozzafava A., Conway J. (ed.): Carbonic Anhydrase: its Inhibitors and Activators. Pp. 1–24. CRC Press, Boca Raton 2004.CrossRefGoogle Scholar
  148. Supuran C.T.: How many carbonic anhydrase inhibition mechanisms exist? - J. Enzym. Inhib. Med. Ch. 31: 345–360, 2016.CrossRefGoogle Scholar
  149. Supuran C.T.: Structure and function of carbonic anhydrases. - Biochem. J. 473: 2023–2032, 2016.PubMedCrossRefGoogle Scholar
  150. Tiwari A., Kumar P., Singh S., Ansari S.A.: Carbonic anhydrase in relation to higher plants. - Photosynthetica 43: 1–11, 2005.CrossRefGoogle Scholar
  151. Tripp B.C., Smith K., Ferry J.G.: Carbonic anhydrase: New insights for an ancient enzyme. - J. Biol. Chem. 276: 48615–48618, 2001.PubMedCrossRefGoogle Scholar
  152. Veitch F.P., Blankenship L.C.: Carbonic anhydrase activity in bacteria. - Nature 197: 76–77, 1963.PubMedCrossRefGoogle Scholar
  153. Vullo D., Del Prete S., Osman S.M. et al.: Sulfonamide inhibition studies of the δ-carbonic anhydrase from the diatom Thalassiosira weissflogii. - Bioorg. Med. Chem. Lett. 24: 275–279, 2014.PubMedCrossRefGoogle Scholar
  154. Woese C.R., Kandler O., Wheelis M.L.: Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. - P. Natl. Acad. Sci. USA 87: 4576–4579, 1990.CrossRefGoogle Scholar
  155. Xu Y., Feng L., Jeffrey P.D. et al.: Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. - Nature 452: 56–61, 2008.PubMedCrossRefGoogle Scholar
  156. Zabaleta E., Martin M.V., Braun H.-P: A basal carbon concentrating mechanism in plants?–Plant Sci. 187: 97–104, 2012.PubMedCrossRefGoogle Scholar
  157. Zavarzin G.A.: The rise of the biosphere. - Microbiology+ 66: 603–611, 1997.Google Scholar
  158. Zavarzin G.A.: Microbial geochemical calcium cycle. - Microbiology+ 71: 1–17, 2002.Google Scholar
  159. Zimmerman S.A., Tomb J.F., Ferry J.G.: Characterization of CamH from Methanosarcina thermophila, founding member of a subclass of the β-class of carbonic anhydrases. - J. Bacteriol. 192: 1353–1360, 2010.PubMedCrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2017

Authors and Affiliations

  1. 1.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations