ISSN (print) 0868-8540, (online) 2413-5984
  • 3 of 7
Algologia 2021, 31(4): 337–352
Physiology, Biochemistry, Biophysics

The roles of carbonic anhydrases in сarbon concentrating mechanisms of aquatic photoautotrophs

Polishchuk O.V.

The article surveys multiple roles of carbonic anhydrases (CAs) in inorganic carbon (Ci) acquisition by cyanobacteria, microalgae, and macrophytes under Ci limiting conditions. Slow Ci diffusion in aquatic environments imposes the need for carbon concentrating mechanisms (also named CO2 concentrating mechanisms, CCMs) in aquatic photoautotrophs to transport Ci against the gradient and ensure CO2 supply to photosynthesis. There are common requirements for efficient CCM functioning in cyanobacteria, algae, and aquatic angiosperms, including active transport of HCO3- to the Ci-concentrating compartment and CO2 generation from the HCO3- pool in the Rubisco-enriched subcompartment. Facilitating Ci diffusion in aqueous solutions and across lipid bilayers, CAs play essential roles in CCMs that are best studied in cyanobacteria, green algae, and diatoms. Roles of CAs in CCMs depend on their localization and include facilitation of active transmembrane Ci uptake by its supplying at the outer surface (Role 1) and removal at the inner surface (Role 2), as well as the acceleration of CO2 production from HCO3- near Rubisco (Role 3) in a special CO2-tight compartment, carboxysome in cyanobacteria or pyrenoid in microalgae. The compartmentalization of CAs is also critical because, if activated in the HCO3- –concentrating compartment, they can easily eliminate the Ci gradient created by CCMs.

Keywords: microalgae, cyanobacteria, macrophytes, photosynthesis, pyrenoid, carboxysome, inorganic carbon, carbon concentrating mechanisms, carbonic anhydrase

Full text: PDF (Rus) 1.00M

  1. Aizawa K., Miyachi S. 1986. Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol. Lett. 39(3): 215–233.–6968.1986.tb01860.x
  2. Badger M. 2003. The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynth. Res. 77(2-3): 83–94.
  3. Badger M.R., Price G.D. 1992. The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol. Plant. 84(4): 606–615.–3054.1992.tb04711.x
  4. Badger M.R., Kaplan A., Berry J.A. 1978. A mechanism for concentrating CO2 in Chlamydomonas reinhardtii and Anabaena variabilis and its role in photosynthetic CO2 fixation. Carnegie Inst. Yearbook. 77: 251–261.
  5. Badger M.R., Andrews T.J., Whitney S.M., Ludwig M., Yellowlees D.C., Leggat W., Price G.D. 1998. The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can. J. Bot. 76(6): 1052–1071.
  6. Battchikova N., Eisenhut M., Aro E.-M. 2011. Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim. Biophys. Acta - Bioenergetics. 1807(8): 935–944.
  7. Berner R.A. 2006. GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochim. Cosmochim. Acta. 70(23): 5653–5664.
  8. Berry J., Farquhar G. 1978. The CO2 concentrating function of C4 photosynthesis. A biochemical model: Proc. 4th Int. Congr. on Photosynthesis (Reading, England, 1977). London: Biochem. Soc. Pp. 119–131.
  9. Blanco-Rivero A., Shutova T., Román M.J., Villarejo A., Martinez F. 2012. Phosphorylation controls the localization and activation of the lumenal carbonic anhydrase in Chlamydomonas reinhardtii. PLoS ONE. 7(11): e49063.
  10. Cannon G.C., Heinhorst S., Kerfeld C.A. 2010. Carboxysomal carbonic anhydrases: structure and role in microbial CO2 fixation. Biochim. Biophys. Acta  Proteins and Proteomics. 1804(2): 382–392.
  11. Coleman J.R. 2000. In: Photosynthesis. Advances in Photosynthesis and Respiration. Vol. 9. Dordrecht: Kluwer Acad. Publ. Pp. 353–367.
  12. DiMario R.J., Machingura M.C., Waldrop G.L., Moroney J.V. 2018. The many types of carbonic anhydrases in photosynthetic organisms. Plant Sci. 268: 11–17.
  13. Giordano M., Beardall J., Raven J.A. 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56: 99–131.
  14. Hagemann M., Kaplan A. 2020. Is the structure of the CO2-hydrating complex I compatible with the cyanobacterial CO2-concentrating mechanism ? Plant Physiol. 183(2): 460–463.
  15. Han X., Sun N., Xu M., Mi H. 2017. Co-ordination of NDH and cup proteins in CO2 uptake in cyanobacterium Synechocystis sp. PCC 6803. J. Exp. Bot. 68(14): 3869–3877.
  16. Hatch M.D. 1987. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta. 895(2): 81–106.
  17. Hirakawa Y., Senda M., Fukuda K., Yu H.Y., Ishida M., Taira M., Kinbara K., Senda T. 2021. Characterization of a novel type of carbonic anhydrase that acts without metal cofactors. BMC Biol. 19: 105. doi: 10.1186/s12915-021-01039-8
  18. Hopkinson B.M., Dupont C.L., Matsuda Y. 2016. The physiology and genetics of CO2 concentrating mechanisms in model diatoms. Curr. Opin. Plant Biol. 31: 51–57.
  19. Huang W., Han S., Jiang H., Gu S., Li W., Gontero B., Maberly S.C. 2020. External α-carbonic anhydrase and solute carrier 4 are required for bicarbonate uptake in a freshwater angiosperm. J. Exp. Bot. 71(19): 6004–6014.
  20. Jensen E.L., Maberly S.C., Gontero B. 2020. Insights on the functions and ecophysiological relevance of the diverse carbonic anhydrases in microalgae. Int. J. Mol. Sci. 21(8): 2922.
  21. Jensen E.L., Clement R., Kosta A., Maberly S.C., Gontero B. 2019. A new widespread subclass of carbonic anhydrase in marine phytoplankton. ISME J. 13(8): 2094–2106.
  22. Jin S., Sun J., Wunder T., Tang D., Cousins A.B., Sze S.K., Mueller-Cajar O., Gao Y.-G. 2016. Structural insights into the LCIB protein family reveals a new group of β-carbonic anhydrases. Proc. Nat Acad. Sci. 113(51): 14716–14721.
  23. Kaplan A., Reinhold L. 1999. CO2 concentrating mechanisms in photosynthetic microorganisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50(1): 539–570.
  24. Kenrick P., Crane P.R. 1997. The origin and early evolution of plants on land. Nature. 389(6646): 33–39.
  25. Kerfeld C.A., Melnicki M.R. 2016. Assembly, function and evolution of cyanobacterial carboxysomes. Curr. Opin. Plant Biol. 31: 66–75.
  26. Kikutani S., Nakajima K., Nagasato C., Tsuji Y., Miyatake A., Matsuda Y. 2016. Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc. Nat. Acad. Sci. 113(35): 9828–9833.
  27. Kimber M.S. 2014. In: Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Dordrecht: Springer Netherlands. Pp. 89–103.
  28. Kupriyanova E., Villarejo A., Markelova A., Gerasimenko L., Zavarzin G., Samuelsson G., Los D.A., Pronina N. 2007. Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology. 153(4): 1149–1156.
  29. Kupriyanova E.V., Sinetova M.A., Markelova A.G., Allakhverdiev S.I., Los D.A., Pronina N.A. 2011. Extracellular β-class carbonic anhydrase of the alkaliphilic cyanobacterium Microcoleus chthonoplastes. J. Photochem. Photobiol. B: Biology. 103(1): 78–86.
  30. Kupriyanova E.V., Sinetova M.A., Mironov K.S., Novikova G.V., Dykman L.A., Rodionova M.V., Gabrielyan D.A., Los D.A. 2019. Highly active extracellular α-class carbonic anhydrase of Cyanothece sp. ATCC 51142. Biochimie. 160: 200–209.
  31. Li T., Sharp C.E., Ataeian M., Strous M., de Beer D. 2018. Role of extracellular carbonic anhydrase in dissolved inorganic carbon uptake in alkaliphilic phototrophic biofilm. Front. Microbiol. 9: 2490.
  32. Mackinder L.C.M. 2018. The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytologist. 217(1): 54–61.
  33. Mackinder L.C.M., Chen C., Leib R.D., Patena W., Blum S.R., Rodman M., Ramundo S., Adams C.M., Jonikas M.C. 2017. A spatial interactome reveals the protein organization of the algal CO2-concentrating mechanism. Cell. 171(1): 133–147.e14.
  34. Maeda S., Badger M.R., Price G.D. 2002. Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942: mechanism of CO2 uptake in cyanobacteria. Mol. Microbiol. 43(2): 425–435.–2958.2002.02753.x
  35. Martin C.L., Tortell P.D. 2008. Bicarbonate transport and extracellular carbonic anhydrase in marine diatoms. Physiol. Plant. 133(1): 106–116.–3054.2008.01054.x
  36. Medina-Puche L., Castelló M.J., Canet J.V., Lamilla J., Colombo M.L., Tornero P. 2017. β-carbonic anhydrases play a role in salicylic acid perception in Arabidopsis. PLoS ONE. 12(7): e0181820.
  37. Morel F.M.M., Lam P.J., Saito M.A. 2020. Trace metal substitution in marine phytoplankton. Annu. Rev. Earth Planet. Sci. 48: 491–517.
  38. Moroney J.V., Ynalvez R.A. 2007. Proposed carbon dioxide concentrating mechanism in Chlamydomonas Reinhardtii. Eukaryot. Cell. 6(8): 1251–1259.
  39. Moroney J.V., Husic H.D., Tolbert N.E. 1985. Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas Reinhardtii. Plant Physiol. 79(1): 177–183.
  40. Peña K.L., Castel S.E., de Araujo C., Espie G.S., Kimber M.S. 2010. Structural basis of the oxidative activation of the carboxysomal γ-carbonic anhydrase, CcmM. Proc. Nat. Acad. Sci. 107(6): 2455–2460.
  41. Polishchuk O.V. 2021. Stress-related changes in the expression and activity of plant carbonic anhydrases. Planta. 253(2): 58.
  42. Poschenrieder C., Fernández J.A., Rubio L., Pérez L., Terés J., Barceló J. 2018. Transport and use of bicarbonate in plants: current knowledge and challenges ahead. Int. J. Mol. Sci. 19(5): 1352.
  43. Price G.D., Badger M.R., Woodger F.J., Long B.M. 2008. 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(7): 1441–1461.
  44. Samukawa M., Shen C., Hopkinson B.M., Matsuda Y. 2014. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosynth. Res. 121(2-3): 235–249.
  45. Sawaya M.R., Cannon G.C., Heinhorst S., Tanaka S., Williams E.B., Yeates T.O., Kerfeld C.A. 2006. The structure of β-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J. Biol. Chem. 281(11): 7546–7555.
  46. Schuller J.M., Saura P., Thiemann J., Schuller S.K., Gamiz-Hernandez A.P., Kurisu G., Nowa-czyk M.M., Kaila V.R.I. 2020. Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I. Nat. Commun. 11(1): 494.
  47. Sun N., Han X., Xu M., Kaplan A., Espie G.S., Mi H. 2019. A thylakoid - located carbonic anhydrase regulates CO2 uptake in the cyanobacterium Synechocystis sp. PCC 6803. New Phytol. 222(1): 206–217.
  48. Tachibana M., Allen A.E., Kikutani S., Endo Y., Bowler C., Matsuda Y. 2011. Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth. Res. 109(1-3): 205–221.
  49. Tchernov D., Helman Y., Keren N., Luz B., Ohad I., Reinhold L., Ogawa T., Kaplan A. 2001. Passive entry of CO2 and its energy-dependent intracellular conversion to HCO3- in cyanobacteria are driven by a Photosystem I-generated ΔμH+. J. Biol. Chem. 276(26): 23450–23455.
  50. Tholen D., Zhu X.-G. 2011. The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol. 156(1): 90–105.
  51. Vats S.K., Kumar S., Ahuja P.S. 2011. CO2 sequestration in plants: lesson from divergent strategies. Photosynthetica. 49(4): 481–496.
  52. von Caemmerer S., Quinn V., Hancock N.C., Price G.D., Furbank R.T., Ludwig M. 2004. Carbonic anhydrase and C4 photosynthesis: a transgenic analysis. Plant, Cell Environ. 27(6): 697–703.–3040.2003.01157.x
  53. Wang Y., Spalding M.H. 2014. Acclimation to very low CO2 : contribution of limiting CO2 inducible proteins, LCIB and LCIA, to inorganic carbon uptake in Chlamydomonas reinhardtii. Plant Physiol. 166(4): 2040–2050.
  54. Xu M., Ogawa T., Pakrasi H.B., Mi H. 2008. Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium, Synechocystis sp. strain PCC 6803. Plant Cell Physiol. 49(6): 994–997.
  55. Yamano T., Tsujikawa T., Hatano K., Ozawa S., Takahashi Y., Fukuzawa H. 2010. Light and low-CO2-dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol. 51(9): 1453–1468.
  56. Ynalvez R.A., Xiao Y., Ward A.S., Cunnusamy K., Moroney J.V. 2008. Identification and characterization of two closely related β-carbonic anhydrases from Chlamydomonas reinhardtii. Physiol. Plant. 133(1): 15–26.–3054.2007.01043.x
  57. Yu J.-W., Price G.D., Song L., Badger M.R. 1992. Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol. 100(2): 794–800.
  58. Zabaleta E., Martin M.V., Braun H.-P. 2012. A basal carbon concentrating mechanism in plants? Plant Sci. 187: 97–104.