1887

Abstract

Carbonic anhydrases (CAs) are metalloenzymes that catalyse the interconversion of carbon dioxide and bicarbonate with high efficiency. This reaction is fundamental to biological processes such as respiration, photosynthesis, pH homeostasis, CO transport and electrolyte secretion. CAs are distributed among all three domains of life, and are currently divided into five evolutionarily unrelated classes (, , , and ). Fungal CAs have only recently been identified and characterized in detail. While and each have only one -CA, multiple copies of -CA- and -CA-encoding genes are found in other fungi. Recent work demonstrates that CAs play an important role in the CO-sensing system of fungal pathogens and in the regulation of sexual development. This review focuses on CA functions in , the fungal pathogens and , and the filamentous ascomycete .

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2010-01-01
2024-04-18
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References

  1. Aguilera J., Petit T., de Winde J. H., Pronk J. T. 2005a; Physiological and genome-wide transcriptional responses of Saccharomyces cerevisiae to high carbon dioxide concentrations. FEMS Yeast Res 5:579–593
    [Google Scholar]
  2. Aguilera J., Van Dijken J. P., De Winde J. H., Pronk J. T. 2005b; Carbonic anhydrase (Nce103p): an essential biosynthetic enzyme for growth of Saccharomyces cerevisiae at atmospheric carbon dioxide pressure. Biochem J 391:311–316
    [Google Scholar]
  3. Amoroso G., Morell-Avrahov L., Müller D., Klug K., Sültemeyer D. 2005; 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
    [Google Scholar]
  4. Anderson P. M., Carlson J. D., Rosenthal G. A., Meister A. 1973; Effect of potassium cyanate on the catalytic activities of carbamyl phosphate synthetase. Biochem Biophys Res Commun 55:246–252
    [Google Scholar]
  5. Anderson P. M., Sung Y. C., Fuchs J. A. 1990; The cyanase operon and cyanate metabolism. FEMS Microbiol Rev 7:247–252
    [Google Scholar]
  6. Bahn Y. S., Mühlschlegel F. A. 2006; CO2 sensing in fungi and beyond. Curr Opin Microbiol 9:572–578
    [Google Scholar]
  7. Bahn Y. S., Cox G. M., Perfect J. R., Heitman J. 2005; Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence. Curr Biol 15:2013–2020
    [Google Scholar]
  8. Bahn Y. S., Xue C., Idnurm A., Rutherford J. C., Heitman J., Cardenas M. E. 2007; Sensing the environment: lessons from fungi. Nat Rev Microbiol 5:57–69
    [Google Scholar]
  9. Chen Y., Cann M. J., Litvin T. N., Iourgenko V., Sinclair M. L., Levin L. R., Buck J. 2000; Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625–628
    [Google Scholar]
  10. Clark D., Rowlett R. S., Coleman J. R., Klessig D. F. 2004; Complementation of the yeast deletion mutant DeltaNCE103 by members of the beta class of carbonic anhydrases is dependent on carbonic anhydrase activity rather than on antioxidant activity. Biochem J 379:609–615
    [Google Scholar]
  11. Cleves A. E., Cooper D. N., Barondes S. H., Kelly R. B. 1996; A new pathway for protein export in Saccharomyces cerevisiae. J Cell Biol 133:1017–1026
    [Google Scholar]
  12. Cronk J. D., Endrizzi J. A., Cronk M. R., O'Neill J. W., Zhang K. Y. 2001; Crystal structure of E. coli beta-carbonic anhydrase, an enzyme with an unusual pH-dependent activity. Protein Sci 10:911–922
    [Google Scholar]
  13. Elleuche S., Pöggeler S. 2008; A cyanase is transcriptionally regulated by arginine and involved in cyanate decomposition in Sordaria macrospora. Fungal Genet Biol 45:1458–1469
    [Google Scholar]
  14. Elleuche S., Pöggeler S. 2009a; Evolution of carbonic anhydrases in fungi. Curr Genet 55:211–222
    [Google Scholar]
  15. Elleuche S., Pöggeler S. 2009b; Beta-carbonic anhydrases play a role in fruiting body development and ascospore germination in the filamentous fungus Sordaria macrospora. PLoS One 4:e5177
    [Google Scholar]
  16. Fabre N., Reiter I. M., Becuwe-Linka N., Genty B., Rumeau D. 2007; Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 30:617–629
    [Google Scholar]
  17. Ferreira F. J., Guo C., Coleman J. R. 2008; Reduction of plastid-localized carbonic anhydrase activity results in reduced Arabidopsis seedling survivorship. Plant Physiol 147:585–594
    [Google Scholar]
  18. Götz R., Gnann A., Zimmermann F. K. 1999; Deletion of the carbonic anhydrase-like gene NCE103 of the yeast Saccharomyces cerevisiae causes an oxygen-sensitive growth defect. Yeast 15:855–864
    [Google Scholar]
  19. Guilloton M., Karst F. 1987; Cyanate specifically inhibits arginine biosynthesis in Escherichia coli K12: a case of by-product inhibition?. J Gen Microbiol 133:655–665
    [Google Scholar]
  20. Guilloton M. B., Lamblin A. F., Kozliak E. I., Gerami-Nejad M., Tu C., Silverman D., Anderson P. M., Fuchs J. A. 1993; A physiological role for cyanate-induced carbonic anhydrase in Escherichia coli. J Bacteriol 175:1443–1451
    [Google Scholar]
  21. Guilloton M., Espie G. S., Anderson P. M. 2002; What is the role of cyanase in plants?. In Reviews in Plant Biochemistry and Biotechnology pp 57–79 Edited by Goyal A., Metha S. L., Lodha M. L.
    [Google Scholar]
  22. Innocenti A., Leewattanapasuk W., Muhlschlegel F. A., Mastrolorenzo A., Supuran C. T. 2009; Carbonic anhydrase inhibitors. Inhibition of the beta-class enzyme from the pathogenic yeast Candida glabrata with anions. Bioorg Med Chem Lett 19:4802–4805
    [Google Scholar]
  23. Jones N. L. 2008; An obsession with CO2 . Appl Physiol Nutr Metab 33:641–650
    [Google Scholar]
  24. Kamerewerd J., Jansson M., Nowrousian M., Pöggeler S., Kück U. 2008; Three alpha-subunits of heterotrimeric G proteins and an adenylyl cyclase have distinct roles in fruiting body development in the homothallic fungus Sordaria macrospora. Genetics 180:191–206
    [Google Scholar]
  25. Kimber M. S., Pai E. F. 2000; The active site architecture of Pisum sativum beta-carbonic anhydrase is a mirror image of that of alpha-carbonic anhydrases. EMBO J 19:1407–1418
    [Google Scholar]
  26. Klengel T., Liang W. J., Chaloupka J., Ruoff C., Schröppel K., Naglik J. R., Eckert S. E., Mogensen E. G., Haynes K. other authors 2005; Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15:2021–2026
    [Google Scholar]
  27. Kück U., Pöggeler S., Nowrousian M., Nolting N., Engh I. 2009; Sordaria macrospora, a model system for fungal development. In The Mycota XV pp 17–39 Edited by Anke T., Weber D. Berlin, Heidelberg: Springer;
    [Google Scholar]
  28. Kusian B., Sültemeyer D., Bowien B. 2002; Carbonic anhydrase is essential for growth of Ralstonia eutropha at ambient CO2 concentrations. J Bacteriol 184:5018–5026
    [Google Scholar]
  29. Li W., Zhou P. P., Jia L. P., Yu L. J., Li X. L., Zhu M. 2009; Limestone dissolution induced by fungal mycelia, acidic materials, and carbonic anhydrase from fungi. Mycopathologia 167:37–46
    [Google Scholar]
  30. Mogensen E. G., Mühlschlegel F. A. 2008; CO2 sensing and virulence of Candida albicans. In The Mycota VI pp 83–94 Edited by Brackhage A. A., Zipfel P. F. Berlin, Heidelberg: Springer;
    [Google Scholar]
  31. Mogensen E. G., Janbon G., Chaloupka J., Steegborn C., Fu M. S., Moyrand F., Klengel T., Pearson D. S., Geeves M. A. other authors 2006; Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 5:103–111
    [Google Scholar]
  32. Nishida H., Beppu T., Ueda K. 2009; Symbiobacterium lost carbonic anhydrase in the course of evolution. J Mol Evol 68:90–96
    [Google Scholar]
  33. Nowrousian M., Würtz C., Pöggeler S., Kück U. 2004; Comparative sequence analysis of Sordaria macrospora and Neurospora crassa as a means to improve genome annotation. Fungal Genet Biol 41:285–292
    [Google Scholar]
  34. Parisi G., Perales M., Fornasari M. S., Colaneri A., González-Schain N., Gómez-Casati D., Zimmermann S., Brennicke A., Araya A. other authors 2004; Gamma carbonic anhydrases in plant mitochondria. Plant Mol Biol 55:193–207
    [Google Scholar]
  35. Pöggeler S., Nowrousian M., Kück U. 2006; Fruiting body development in ascomycetes. In The Mycota I pp 325–355 Edited by Kües U., Fischer R. Berlin & Heidelberg: Springer;
    [Google Scholar]
  36. Sawaya M. R., Cannon G. C., Heinhorst S., Tanaka S., Williams E. B., Yeates T. O., Kerfeld C. A. 2006; 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 281:7546–7555
    [Google Scholar]
  37. Schlicker C., Hall R. A., Vullo D., Middelhaufe S., Gertz M., Supuran C. T., Mühlschlegel F. A., Steegborn C. 2009; Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. J Mol Biol 385:1207–1220
    [Google Scholar]
  38. Slaymaker D. H., Navarre D. A., Clark D., del Pozo O., Martin G. B., Klessig D. F. 2002; The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci U S A 99:11640–11645
    [Google Scholar]
  39. Supuran C. T. 2008; Carbonic anhydrases – an overview. Curr Pharm Des 14:603–614
    [Google Scholar]
  40. Tripp B. C., Smith K., Ferry J. G. 2001; Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276:48615–48618
    [Google Scholar]
  41. Wistrand P. J. 1981; The importance of carbonic anhydrase B and C for the unloading of CO2 by the human erythrocyte. Acta Physiol Scand 113:417–426
    [Google Scholar]
  42. Xu Y., Feng L., Jeffrey P. D., Shi Y., Morel F. M. 2008; Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61
    [Google Scholar]
  43. Ynalvez R. A., Xiao Y., Ward A. S., Cunnusamy K., Moroney J. V. 2008; Identification and characterization of two closely related beta-carbonic anhydrases from Chlamydomonas reinhardtii. Physiol Plant 133:15–26
    [Google Scholar]
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