The structure, kinetics and interactions of the β-carboxysomal β-carbonic anhydrase, CcaA

Biochemical Journal

Volumn 473, Issue 24, 2016, Pages 4559-4572

  Mcgurn, Leah D ^a   Moazami Goudarzi, Maryam ^b   White, Sean A ^a   Suwal, Tannu ^b   Brar, Beant ^b   Tang, Jason Q ^b   Espie, George S ^b   Kimber, Matthew S ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CARBOXYSOMAL BETA CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE; DIMER; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SURFACE PLASMON RESONANCE; SYNECHOCYSTIS SP. PCC 6803; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; KINETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; SYNECHOCOCCUS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CARBONIC ANHYDRASES; CRYSTALLOGRAPHY, X-RAY; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; SURFACE PLASMON RESONANCE; SYNECHOCOCCUS;

EID: 85009477091     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160773     Document Type: Article

References (39)

1. Espie, G.S. and Kimber, M.S. (2011) Carboxysomes: cyanobacterial RubisCO comes in small packages. Photosyn. Res. 109, 7-20 doi:10.1007/s11120-011-9656-y.
2. Rae, B.D., Long, B.M., Whitehead, L.F., Förster, B., Badger, M.R. and Price, G.D. (2013) Cyanobacterial carboxysomes: microcompartments that facilitate CO2 fixation. J. Mol. Microbiol. Biotechnol. 23, 300-307 doi:10.1159/000351342.
3. Kupriyanova, E.V., Sinetova, M.A., Cho, S.M., Park, Y.-I., Los, D.A. and Pronina, N.A. (2013) CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin. Photosyn. Res. 117, 133-146 doi:10.1007/s11120-013-9860-z.
4. Price, G.D. and Badger, M.R. (1989) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-requiring phenotype: evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol. 91, 505-513 doi:10.1104/pp.91.2.505.
5. So, A.K.-C., Espie, G.S., Williams, E.B., Shively, J.M., Heinhorst, S. and Cannon, G.C. (2004) A novel evolutionary lineage of carbonic anhydrase (epsilon class) is a component of the carboxysome shell. J. Bacteriol. 186, 623-630 doi:10.1128/JB.186.3.623-630.2004.
6. Sawaya, M.R., Cannon, G.C., Heinhorst, S., Tanaka, S., Williams, E.B., Yeates, T.O. et al. (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, 7546-7555 doi:10.1074/jbc.M510464200.
7. Heinhorst, S., Williams, E.B., Cai, F., Murin, C.D., Shively, J.M. and Cannon, G.C. (2006) Characterization of the carboxysomal carbonic anhydrase CsoSCA from Halothiobacillus neapolitanus. J. Bacteriol. 188, 8087-8094 doi:10.1128/JB.00990-06.
8. Fukuzawa, H., Suzuki, E., Komukai, Y. and Miyachi, S. (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Proc. Natl. Acad. Sci U.S.A. 89, 4437-4441 doi:10.1073/pnas.89.10.4437.
9. Yu, J.-W., Price, G.D., Song, L. and Badger, M.R. (1992) Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol. 100, 794-800 doi:10.1104/pp.100.2.794.
10. Kimber, M.S. and Pai, E.F. (2000) The active site architecture of Pisum sativum β-carbonic anhydrase is a mirror image of that of α-carbonic anhydrases. EMBO J. 19, 1407-1418 doi:10.1093/emboj/19.7.1407.
11. Long, B.M., Badger, M.R., Whitney, S.M. and Price, G.D. (2007) Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J. Biol. Chem. 282, 29323-29335 doi:10.1074/jbc.M703896200.
12. Long, B.M., Tucker, L., Badger, M.R. and Price, G.D. (2010) Functional cyanobacterial beta-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol. 153, 285-293 doi:10.1104/pp.110.154948.
13. Long, B.M., Rae, B.D., Badger, M.R. and Price, G.D. (2011) Over-expression of the β-carboxysomal CcmM protein in Synechococcus PCC7942 reveals a tight co-regulation of carboxysomal carbonic anhydrase (CcaA) and M58 content. Photosyn. Res. 109, 33-45 doi:10.1007/s11120-011-9659-8.
14. Cot, S.S.-W., So, A.K.-C. and Espie, G.S. (2008) A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. J. Bacteriol. 190, 936-945 doi:10.1128/JB.01283-07.
15. Espie, G.S. and So, A.K.-C. (2005) Cyanobacterial carbonic anhydrases. Can. J. Bot. 83, 721-734 doi:10.1139/b05-907.
16. Peña, K.L., Castel, S.E., de Araujo, C., Espie, G.S. and Kimber, M.S. (2010) Structural basis of the oxidative activation of the carboxysomal γ-carbonic anhydrase, CcmM. Proc. Natl Acad. Sci. U.S.A. 107, 2455-2460 doi:10.1073/pnas.0910866107.
17. de Araujo, C., Arefeen, D., Tadesse, Y., Long, B.M., Price, G.D., Rowlett, R.S. et al. (2014) Identification and characterization of a carboxysomal γ-carbonic anhydrase from the cyanobacterium Nostoc sp. PCC 7120. Photosyn. Res. 121, 135-150 doi:10.1007/s11120-014-0018-4.
18. Kinney, J.N., Salmeen, A., Cai, F. and Kerfeld, C.A. (2012) Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J. Biol. Chem. 287, 17729-17736 doi:10.1074/jbc.M112.355305.
19. Ahnert, S.E., Marsh, J.A., Hernández, H., Robinson, C.V. and Teichmann, S.A. (2015) Principles of assembly reveal a periodic table of protein complexes. Science 350, 2245 doi:10.1126/science.aaa2245.
20. Schlicker, C., Hall, R.A., Vullo, D., Middelhaufe, S., Gertz, M., Supuran, C.T. et al. (2009) Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. Structure 385, 1207-1220 doi:10.1016/j.jmb.2008.11.037.
21. Cronk, J.D., Endrizzi, J.A., Cronk, M.R., O'neill, J.W. and Zhang, K.Y.J. (2001) Crystal structure of E. coli β-carbonic anhydrase, an enzyme with an unusual pH-dependent activity. Protein Sci. 10, 911-922 doi:10.1110/ps.46301.
22. Kabsch, W. (2010) XDS. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 125-132 doi:10.1107/S0907444909047337.
23. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 doi:10.1107/S0021889807021206.
24. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132 doi:10.1107/S0907444904019158.
25. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.-W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W. et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 58, 1948-1954 PMID:12393927.
26. Gray, J.J., Moughon, S., Wang, C., Schueler-Furman, O., Kuhlman, B., Rohl, C.A. et al. (2003) Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J. Mol. Biol. 331, 281-299 doi:10.1016/S0022-2836(03)00670-3.
27. Teng, Y.-B., Jiang, Y.-L., He, Y.-X., He, W.-W., Lian, F.-M., Chen, Y. et al. (2009) Structural insights into the substrate tunnel of Saccharomyces cerevisiae carbonic anhydrase Nce103. BMC Struct. Biol. 9, 67 doi:10.1186/1472-6807-9-67.
28. Cronk, J.D., Rowlett, R.S., Zhang, K.Y.J., Tu, C., Endrizzi, J.A., Lee, J. et al. (2006) Identification of a novel noncatalytic bicarbonate binding site in eubacterial β-carbonic anhydrase. Biochemistry 45, 4351-4361 doi:10.1021/bi052272q.
29. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 doi:10.1016/j.jmb.2007.05.022.
30. Smith, K.S., Ingram-Smith, C. and Ferry, J.G. (2002) Roles of the conserved aspartate and arginine in the catalytic mechanism of an archaeal β-class carbonic anhydrase. J. Bacteriol. 184, 4240-4245 doi:10.1128/JB.184.15.4240-4245.2002.
31. Rowlett, R.S., Tu, C., McKay, M.M., Preiss, J.R., Loomis, R.J., Hicks, K.A. et al. (2002) Kinetic characterization of wild-Type and proton transfer-impaired variants of β-carbonic anhydrase from Arabidopsis thaliana. Arch Biochem. Biophys. 404, 197-209 doi:10.1016/S0003-9861(02)00243-6.
32. Rowlett, R.S., Tu, C., Murray, P.S. and Chamberlin, J.E. (2004) Examination of the role of Gln-158 in the mechanism of CO2 hydration catalyzed by β-carbonic anhydrase from Arabidopsis thaliana. Arch Biochem. Biophys. 425, 25-32 doi:10.1016/j.abb.2004.02.033.
33. Aggarwal, M., Chua, T.K., Pinard, M.A., Szebenyi, D.M. and McKenna, R. (2015) Carbon dioxide 'Trapped' in a β-carbonic anhydrase. Biochemistry 54, 6631-6638 doi:10.1021/acs.biochem.5b0098734.
34. Rowlett, R.S. (2010) Structure and catalytic mechanism of the beta-carbonic anhydrases. Biochim. Biophys. Acta 1804, 362-373 doi:10.1016/j.bbapap.2009.08.002.
35. Covarrubias, A.S., Bergfors, T., Jones, T.A. and Högbom, M. (2006) Structural mechanics of the pH-dependent activity of β-carbonic anhydrase from Mycobacterium tuberculosis. J. Biol. Chem. 281, 4993-4999 doi:10.1074/jbc.M510756200.
36. Strop, P., Smith, K.S., Iverson, T.M., Ferry, J.G. and Rees, D.C. (2001) Crystal structure of the 'cab-' type β class carbonic anhydrase from the archaeon Methanobacterium thermoautotrophicum. J. Biol. Chem. 276, 10299-10305 doi:10.1074/jbc.M009182200.
37. Smeulders, M.J., Barensds, T.R.M., Pol, A., Scherer, A., Zandvoort, M.H., Udvarhelyi, A. et al. (2011) Evolution of a new enzyme for carbon disulphide conversion by an acidothermophilic archaeon. Nature 478, 412-416 doi:10.1038/nature10464.
38. So, A.K.-C., Cot, S.S.-W. and Espie, G.S. (2002) Characterization of the C-Terminal extension of carboxysomal carbonic anhydrase from Synechocystis sp. PCC6803. Funct. Plant Biol. 29, 183-194 doi:10.1071/PP01179.
39. So, A.K.-C. (2004) The role of carbonic anhydrase in the CO2-concentrating mechanism of cyanobacteria. Ph.D. Thesis, University of Toronto.