This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by So, A. K.-C.
Right arrow Articles by Cannon, G. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by So, A. K.-C.
Right arrow Articles by Cannon, G. C.

 Previous Article  |  Next Article 

Journal of Bacteriology, February 2004, p. 623-630, Vol. 186, No. 3
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.3.623-630.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

A Novel Evolutionary Lineage of Carbonic Anhydrase ({varepsilon} Class) Is a Component of the Carboxysome Shell

Anthony K.-C. So,1 George S. Espie,1 Eric B. Williams,2 Jessup M. Shively,2,3 Sabine Heinhorst,2 and Gordon C. Cannon2*

Department of Botany, University of Toronto at Mississauga, Mississauga, Ontario, L5L 1C6, Canada,1 Department of Chemistry and Biochemistry, The University of Southern Mississippi, Hattiesburg, Mississippi 39406-5043,2 Department of Genetics and Biochemistry, Clemson University, Clemson, South Carolina 296343

Received 3 September 2003/ Accepted 29 October 2003

A significant portion of the total carbon fixed in the biosphere is attributed to the autotrophic metabolism of prokaryotes. In cyanobacteria and many chemolithoautotrophic bacteria, CO2 fixation is catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), most if not all of which is packaged in protein microcompartments called carboxysomes. These structures play an integral role in a cellular CO2-concentrating mechanism and are essential components for autotrophic growth. Here we report that the carboxysomal shell protein, CsoS3, from Halothiobacillus neapolitanus is a novel carbonic anhydrase ({varepsilon}-class CA) that has an evolutionary lineage distinct from those previously recognized in animals, plants, and other prokaryotes. Functional CAs encoded by csoS3 homologues were also identified in the cyanobacteria Prochlorococcus sp. and Synechococcus sp., which dominate the oligotrophic oceans and are major contributors to primary productivity. The location of the carboxysomal CA in the shell suggests that it could supply the active sites of RuBisCO in the carboxysome with the high concentrations of CO2 necessary for optimal RuBisCO activity and efficient carbon fixation in these prokaryotes, which are important contributors to the global carbon cycle.

* Corresponding author. Mailing address: Department of Chemistry and Biochemistry, The University of Southern Mississippi, Charles Lane Drive, Hattiesburg, MS 39406-5043. Phone: (601) 266-4221. Fax: (601) 266-6075. E-mail: gordon.cannon{at}usm.edu.

Journal of Bacteriology, February 2004, p. 623-630, Vol. 186, No. 3
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.3.623-630.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Scanlan, D. J., Ostrowski, M., Mazard, S., Dufresne, A., Garczarek, L., Hess, W. R., Post, A. F., Hagemann, M., Paulsen, I., Partensky, F. (2009). Ecological Genomics of Marine Picocyanobacteria. Microbiol. Mol. Biol. Rev. 73: 249-299 [Abstract] [Full Text]  
  • Moya, A., Tambutte, S., Bertucci, A., Tambutte, E., Lotto, S., Vullo, D., Supuran, C. T., Allemand, D., Zoccola, D. (2008). Carbonic Anhydrase in the Scleractinian Coral Stylophora pistillata: CHARACTERIZATION, LOCALIZATION, AND ROLE IN BIOMINERALIZATION. J. Biol. Chem. 283: 25475-25484 [Abstract] [Full Text]  
  • Lapointe, M., MacKenzie, T. D.B., Morse, D. (2008). An External {delta}-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition. Plant Physiol. 147: 1427-1436 [Abstract] [Full Text]  
  • 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: 1441-1461 [Abstract] [Full Text]  
  • Dou, Z., Heinhorst, S., Williams, E. B., Murin, C. D., Shively, J. M., Cannon, G. C. (2008). CO2 Fixation Kinetics of Halothiobacillus neapolitanus Mutant Carboxysomes Lacking Carbonic Anhydrase Suggest the Shell Acts as a Diffusional Barrier for CO2. J. Biol. Chem. 283: 10377-10384 [Abstract] [Full Text]  
  • Tanaka, S., Kerfeld, C. A., Sawaya, M. R., Cai, F., Heinhorst, S., Cannon, G. C., Yeates, T. O. (2008). Atomic-Level Models of the Bacterial Carboxysome Shell. Science 319: 1083-1086 [Abstract] [Full Text]  
  • Cot, S. S.-W., So, A. K.-C., Espie, G. S. (2008). A Multiprotein Bicarbonate Dehydration Complex Essential to Carboxysome Function in Cyanobacteria. J. Bacteriol. 190: 936-945 [Abstract] [Full Text]  
  • Bury-Mone, S., Mendz, G. L., Ball, G. E., Thibonnier, M., Stingl, K., Ecobichon, C., Ave, P., Huerre, M., Labigne, A., Thiberge, J.-M., De Reuse, H. (2008). Roles of {alpha} and Carbonic Anhydrases of Helicobacter pylori in the Urease-Dependent Response to Acidity and in Colonization of the Murine Gastric Mucosa. Infect. Immun. 76: 497-509 [Abstract] [Full Text]  
  • Tchernov, D., Lipschultz, F. (2008). Carbon isotopic composition of Trichodesmium spp. colonies off Bermuda: effects of colony mass and season. J PLANKTON RES 30: 21-31 [Abstract] [Full Text]  
  • Long, B. M., Badger, M. R., Whitney, S. M., 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 [Abstract] [Full Text]  
  • Moroney, J. V., Ynalvez, R. A. (2007). Proposed Carbon Dioxide Concentrating Mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6: 1251-1259 [Full Text]  
  • Tetu, S. G., Tanz, S. K., Vella, N., Burnell, J. N., Ludwig, M. (2007). The Flaveria bidentis beta-Carbonic Anhydrase Gene Family Encodes Cytosolic and Chloroplastic Isoforms Demonstrating Distinct Organ-Specific Expression Patterns. Plant Physiol. 144: 1316-1327 [Abstract] [Full Text]  
  • 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: 1149-1156 [Abstract] [Full Text]  
  • Heinhorst, S., Williams, E. B., Cai, F., Murin, C. D., Shively, J. M., Cannon, G. C. (2006). Characterization of the Carboxysomal Carbonic Anhydrase CsoSCA from Halothiobacillus neapolitanus. J. Bacteriol. 188: 8087-8094 [Abstract] [Full Text]  
  • Soto, A. R., Zheng, H., Shoemaker, D., Rodriguez, J., Read, B. A., Wahlund, T. M. (2006). Identification and Preliminary Characterization of Two cDNAs Encoding Unique Carbonic Anhydrases from the Marine Alga Emiliania huxleyi. Appl. Environ. Microbiol. 72: 5500-5511 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Beller, H. R., Chain, P. S. G., Letain, T. E., Chakicherla, A., Larimer, F. W., Richardson, P. M., Coleman, M. A., Wood, A. P., Kelly, D. P. (2006). The Genome Sequence of the Obligately Chemolithoautotrophic, Facultatively Anaerobic Bacterium Thiobacillus denitrificans. J. Bacteriol. 188: 1473-1488 [Abstract] [Full Text]  
  • Badger, M. R., Price, G. D., Long, B. M., Woodger, F. J. (2006). The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57: 249-265 [Abstract] [Full Text]  
  • Dobrinski, K. P., Longo, D. L., Scott, K. M. (2005). The Carbon-Concentrating Mechanism of the Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena. J. Bacteriol. 187: 5761-5766 [Full Text]  
  • Kerfeld, C. A., Sawaya, M. R., Tanaka, S., Nguyen, C. V., Phillips, M., Beeby, M., Yeates, T. O. (2005). Protein Structures Forming the Shell of Primitive Bacterial Organelles. Science 309: 936-938 [Abstract] [Full Text]  
  • Wahlund, T. M., Zhang, X., Read, B. A. (2004). Expressed sequence tag profiles from calcifying and non-calcifying cultures of Emiliania huxleyi. Micropaleontology 50: 145-155 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»