The roles of carbonic anhydrases in сarbon concentrating mechanisms of aquatic photoautotrophs
Section:
Physiology, Biochemistry. BiophysicsIssue:
Vol. 31 No. 4 (2021)Pages:
337–352DOI:
https://doi.org/10.15407/alg31.04.337Abstract
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, carbonic anhydrase, carbon concentrating mechanismsFull text
References
Aizawa K., Miyachi S. 1986. Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol. Lett. 39(3): 215–233. https://doi.org/10.1111/j.1574–6968.1986.tb01860.x
Badger M. 2003. The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynth. Res. 77(2-3): 83–94. https://doi.org/10.1023/A:1025821717773 https://www.ncbi.nlm.nih.gov/pubmed/16228367
Badger M.R., Price G.D. 1992. The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol. Plant. 84(4): 606–615. https://doi.org/10.1111/j.1399–3054.1992.tb04711.x
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.
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. https://doi.org/10.1139/b98-074
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. https://doi.org/10.1016/j.bbabio.2010.10.017 https://www.ncbi.nlm.nih.gov/pubmed/21035426
Berner R.A. 2006. GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochim. Cosmochim. Acta. 70(23): 5653–5664. https://doi.org/10.1088/1126-6708/2005/11/032
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.
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. https://doi.org/10.1371/journal.pone.0049063 https://www.ncbi.nlm.nih.gov/pubmed/23139834 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3490910
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. https://doi.org/10.1016/j.bbapap.2009.09.026 https://www.ncbi.nlm.nih.gov/pubmed/19818881
Coleman J.R. 2000. In: Photosynthesis. Advances in Photosynthesis and Respiration. Vol. 9. Dordrecht: Kluwer Acad. Publ. Pp. 353–367. https://doi.org/10.1007/0-306-48137-5_15
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. https://doi.org/10.1016/j.plantsci.2017.12.002 https://www.ncbi.nlm.nih.gov/pubmed/29362079
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. https://doi.org/10.1146/annurev.arplant.56.032604.144052 https://www.ncbi.nlm.nih.gov/pubmed/15862091
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. https://doi.org/10.1104/pp.20.00220 https://www.ncbi.nlm.nih.gov/pubmed/32213538 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7271811
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. https://doi.org/10.1093/jxb/erx129 https://www.ncbi.nlm.nih.gov/pubmed/28911053 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5853218
Hatch M.D. 1987. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta. 895(2): 81–106. https://doi.org/10.1016/S0304-4173(87)80009-5
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 https://www.ncbi.nlm.nih.gov/pubmed/34006275 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8132391
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. https://doi.org/10.1016/j.pbi.2016.03.013 https://www.ncbi.nlm.nih.gov/pubmed/27055267
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. https://doi.org/10.1093/jxb/eraa351 https://www.ncbi.nlm.nih.gov/pubmed/32721017
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. https://doi.org/10.3390/ijms21082922 https://www.ncbi.nlm.nih.gov/pubmed/32331234 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7215798
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. https://doi.org/10.1038/s41396-019-0426-8 https://www.ncbi.nlm.nih.gov/pubmed/31024153 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776030
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. https://doi.org/10.1073/pnas.1616294113. https://www.ncbi.nlm.nih.gov/pubmed/27911826 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5187666
Kaplan A., Reinhold L. 1999. CO2 concentrating mechanisms in photosynthetic microorganisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50(1): 539–570. https://doi.org/10.1146/annurev.arplant.50.1.539 https://www.ncbi.nlm.nih.gov/pubmed/15012219
Kenrick P., Crane P.R. 1997. The origin and early evolution of plants on land. Nature. 389(6646): 33–39. https://doi.org/10.1038/37918
Kerfeld C.A., Melnicki M.R. 2016. Assembly, function and evolution of cyanobacterial carboxysomes. Curr. Opin. Plant Biol. 31: 66–75. https://doi.org/10.1016/j.pbi.2016.03.009 https://www.ncbi.nlm.nih.gov/pubmed/27060669
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. https://doi.org/10.1073/pnas.1603112113 https://www.ncbi.nlm.nih.gov/pubmed/27531955 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5024579
Kimber M.S. 2014. In: Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Dordrecht: Springer Netherlands. Pp. 89–103. https://doi.org/10.1007/978-94-007-7359-2_6 https://www.ncbi.nlm.nih.gov/pubmed/24146376
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. https://doi.org/10.1099/mic.0.2006/003905-0 https://www.ncbi.nlm.nih.gov/pubmed/17379724
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. https://doi.org/10.1016/j.jphotobiol.2011.01.021 https://www.ncbi.nlm.nih.gov/pubmed/21330147
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. https://doi.org/10.1016/j.biochi.2019.03.009 https://www.ncbi.nlm.nih.gov/pubmed/30898645
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. https://doi.org/10.3389/fmicb.2018.02490 https://www.ncbi.nlm.nih.gov/pubmed/30405559 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6204761
Mackinder L.C.M. 2018. The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytologist. 217(1): 54–61. https://doi.org/10.1111/nph.14749 https://www.ncbi.nlm.nih.gov/pubmed/28833179
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. https://doi.org/10.1016/j.cell.2017.08.044 https://www.ncbi.nlm.nih.gov/pubmed/28938113 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5616186
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. https://doi.org/10.1046/j.1365–2958.2002.02753.x https://www.ncbi.nlm.nih.gov/pubmed/11985719
Martin C.L., Tortell P.D. 2008. Bicarbonate transport and extracellular carbonic anhydrase in marine diatoms. Physiol. Plant. 133(1): 106–116. https://doi.org/10.1111/j.1399–3054.2008.01054.x https://www.ncbi.nlm.nih.gov/pubmed/18298417
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. https://doi.org/10.1371/journal.pone.0181820 https://www.ncbi.nlm.nih.gov/pubmed/28753666 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5533460
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. https://doi.org/10.1146/annurev-earth-053018-060108
Moroney J.V., Ynalvez R.A. 2007. Proposed carbon dioxide concentrating mechanism in Chlamydomonas Reinhardtii. Eukaryot. Cell. 6(8): 1251–1259. https://doi.org/10.1128/EC.00064-07 https://www.ncbi.nlm.nih.gov/pubmed/17557885 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1951128
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. https://doi.org/10.1104/pp.79.1.177 https://www.ncbi.nlm.nih.gov/pubmed/16664365 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1074847
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. https://doi.org/10.1073/pnas.0910866107 https://www.ncbi.nlm.nih.gov/pubmed/20133749 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2823891
Polishchuk O.V. 2021. Stress-related changes in the expression and activity of plant carbonic anhydrases. Planta. 253(2): 58. https://doi.org/10.1007/s00425-020-03553-5 https://www.ncbi.nlm.nih.gov/pubmed/33532871
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. https://doi.org/10.3390/ijms19051352 https://www.ncbi.nlm.nih.gov/pubmed/29751549 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5983714
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. https://doi.org/10.1093/jxb/erm112 https://www.ncbi.nlm.nih.gov/pubmed/17578868
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. https://doi.org/10.1007/s11120-014-9967-x https://www.ncbi.nlm.nih.gov/pubmed/24414291
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. https://doi.org/10.1074/jbc.M510464200 https://www.ncbi.nlm.nih.gov/pubmed/16407248
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. https://doi.org/10.1038/s41467-020-14347-4 https://www.ncbi.nlm.nih.gov/pubmed/31980611 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6981117
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. https://doi.org/10.1111/nph.15575 https://www.ncbi.nlm.nih.gov/pubmed/30383301
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. https://doi.org/10.1007/s11120-011-9634-4 https://www.ncbi.nlm.nih.gov/pubmed/21365259
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. https://doi.org/10.1074/jbc.M101973200 https://www.ncbi.nlm.nih.gov/pubmed/11297562
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. https://doi.org/10.1104/pp.111.172346 https://www.ncbi.nlm.nih.gov/pubmed/21441385 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3091052
Vats S.K., Kumar S., Ahuja P.S. 2011. CO2 sequestration in plants: lesson from divergent strategies. Photosynthetica. 49(4): 481–496. https://doi.org/10.1007/s11099-011-0078-z
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. https://doi.org/10.1111/j.1365–3040.2003.01157.x
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. https://doi.org/10.1104/pp.114.248294 https://www.ncbi.nlm.nih.gov/pubmed/25336519 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4256846
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. https://doi.org/10.1093/pcp/pcn074 https://www.ncbi.nlm.nih.gov/pubmed/18467341
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. https://doi.org/10.1093/pcp/pcq105 https://www.ncbi.nlm.nih.gov/pubmed/20660228
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. https://doi.org/10.1111/j.1399–3054.2007.01043.x https://www.ncbi.nlm.nih.gov/pubmed/18405332
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. https://doi.org/10.1104/pp.100.2.794 https://www.ncbi.nlm.nih.gov/pubmed/16653060 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1075628
Zabaleta E., Martin M.V., Braun H.-P. 2012. A basal carbon concentrating mechanism in plants? Plant Sci. 187: 97–104. https://doi.org/10.1016/j.plantsci.2012.02.001 https://www.ncbi.nlm.nih.gov/pubmed/22404837
