Skip to main content
SpringerLink
Log in

Carboxysomes – Sequestering RubisCO for Efficient Carbon Fixation

  • Chapter
  • First Online:
The Structural Basis of Biological Energy Generation

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 39))

Summary

Carbon fixation in cyanobacteria (and some chemoautotrophs) occurs in large cytoplasmic bodies known as carboxysomes. Carboxysomes are organized as an enzymatic core comprised of RubisCO and carbonic anhydrase, encapsulated within a thin protein shell. The carbonic anhydrase converts concentrated bicarbonate into carbon dioxide, which can then be fixed by RubisCO. The shell is required as it presents a semi-permeable barrier; in its absence, CO2 would escape too rapidly to allow efficient fixation. Despite the complexity of this arrangement, and large size of the resulting particle (90–400 nm), carboxysomes are self-organizing and require as few as eight different polypeptides (including the enzymes) for proper self-assembly. This chapter explores discusses the structure and functional roles of the proteins that build up the carboxysome, and analyses the unique architecture of these particles.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BMC:

– Bacterial microcompartment;

CA:

– Carbonic anhydrase;

DPB:

– Doubled permuted bacterial microcompartment;

etu:

– Ethanolamine utilization microcompartment;

pdu:

– Propanediol utilization microcompartment;

3PGA:

– 3-Phosphoglycerate;

RuBP:

– Ribulose 1,5-bisphosphate;

RubisCO:

– Ribulose 1,5-bisphosphate carboxylase/oxygenase

References

  • Alber BE, Ferry JG (1994) A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci U S A 91:6909–6913

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baker SH, Lorbach SC, Rodriguez-Buey M, Williams DS, Aldrich HC, Shively JM (1999) The correlation of the gene csoS2 of the carboxysome operon with two polypeptides of the carboxysome in Thiobacillus neapolitanus. Arch Microbiol 172:233–239

    Article  CAS  PubMed  Google Scholar 

  • Baker SH, Williams DS, Aldrich HC, Gambrell AC, Shively JM (2000) Identification and localization of the carboxysome peptide Csos3 and its corresponding gene in Thiobacillus neapolitanus. Arch Microbiol 173:278–283

    Article  CAS  PubMed  Google Scholar 

  • Bonacci W, Teng PK, Afonso B, Niederholtmeyer H, Grob P, Silver PA, Savage DF (2012) Modularity of a carbon-fixing protein organelle. Proc Natl Acad Sci U S A 109:478–483

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cai F, Menon BB, Cannon GC, Curry KJ, Shively JM, Heinhorst S (2009) The pentameric vertex proteins are necessary for the icosahedral carboxysome shell to function as a CO2 leakage barrier. PLoS ONE 4:e7521

    Article  PubMed Central  PubMed  Google Scholar 

  • Cannon GC, Heinhorst S, Bradburne CE, Shively JM (2002) Carboxysome genomics: a status report. Funct Plant Biol 29:175–182

    Article  CAS  Google Scholar 

  • Cot SS-W, So AKC, Espie GS (2008) A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. J Bacteriol 190:936–945

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crowley CS, Sawaya MR, Bobik TA, Yeates TO (2008) Structure of the PduU shell protein from the Pdu microcompartment of Salmonella. Structure 16:1324–1332

    Article  CAS  PubMed  Google Scholar 

  • Danziger O (2003) Conversion of the allosteric transition of GroEL from concerted to sequential by the single mutation Asp-155 -> Ala. Proc Natl Acad Sci U S A 100:13797–13802

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC (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

    Article  CAS  PubMed  Google Scholar 

  • Dryden KA, Crowley CS, Tanaka S, Yeates TO, Yeager M (2009) Two-dimensional crystals of carboxysome shell proteins recapitulate the hexagonal packing of three-dimensional crystals. Protein Sci 18:2629–2635

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Espie GS, Kimber MS (2011) Carboxysomes: cyanobacterial RubisCO comes in small packages. Photosynth Res 109:7–20

    Article  CAS  PubMed  Google Scholar 

  • Ferry JG (2010) The gamma class of carbonic anhydrases. Biochim Biophys Acta 1804:374–381

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Friedberg D, Kaplan A, Ariel R, Kessel M, Seijffers J (1989) The 5′-flanking region of the gene encoding the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is crucial for growth of the cyanobacterium Synechococcus sp. strain PCC 7942 at the level of CO2 in air. J Bacteriol 171:6069–6076

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fukuzawa H, Suzuki E, Komukai Y, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gonzales AD, Light YK, Zhang Z, Iqbal T, Lane TW, Martino A (2005) Proteomic analysis of the CO2-concentrating mechanism in the open-ocean cyanobacterium Synechococcus WH8102. Can J Bot 83:735–745

    Article  CAS  Google Scholar 

  • Iancu CV, Ding HJ, Morris DM, Dias DP, Gonzales AD, Martino A, Jensen GJ (2007) The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography. J Mol Biol 372:764–773

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaneko Y, Danev R, Nagayama K, Nakamoto H (2006) Intact carboxysomes in a cyanobacterial cell visualized by Hilbert differential contrast transmission electron microscopy. J Bacteriol 188:805–808

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kerfeld CA, Sawaya MR, Tanaka S, Nguyen CV, Phillips M, Beeby M, Yeates TO (2005) Protein structures forming the shell of primitive bacterial organelles. Science 309:936–938

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA, Heinhorst S, Cannon GC (2010) Bacterial microcompartments. Annu Rev Microbiol 64:391–408

    Article  CAS  PubMed  Google Scholar 

  • Kimber MS, Pai EF (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kinney JN, Salmeen A, Cai F, Kerfeld CA (2012) Elucidating the essential role of the conserved carboxysomal protein CcmN reveals a common feature of bacterial microcompartment assembly. J Biol Chem 287:17729–17736

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kisker C, Schindelin H, Alber BE, Ferry JG, Rees DC (1996) A left-hand beta-helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila. EMBO J 15:2323–2330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klein MG, Zwart P, Bagby SC, Cai F, Chisholm SW, Heinhorst S, Cannon GC, Kerfeld CA (2009) Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport. J Mol Biol 392:319–333

    Article  CAS  PubMed  Google Scholar 

  • Long BM, Price GD, Badger MR (2005) Proteomic assessment of an established technique for carboxysome enrichment from Synechococcus PCC7942. Can J Bot 83:746–757

    Article  CAS  Google Scholar 

  • Long BM, Badger MR, Whitney SM, Price GD (2007) Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282:29323–29335

    Article  CAS  PubMed  Google Scholar 

  • Long BM, Tucker L, Badger MR, Price GD (2010) Functional cyanobacterial beta-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153:285–293

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Menon BB, Dou Z, Heinhorst S, Shively JM, Cannon GC (2008) Halothiobacillus neapolitanus carboxysomes sequester heterologous and chimeric RubisCO species. PLoS ONE 3:e3570

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 (supplement). DNA Res 9:135–148

    Article  CAS  PubMed  Google Scholar 

  • Peña KL, Castel SE, De Araujo C, Espie GS, Kimber MS (2010) Structural basis of the oxidative activation of the carboxysomal -carbonic anhydrase, CcmM. Proc Natl Acad Sci U S A 107:2455–2460

    Article  PubMed Central  PubMed  Google Scholar 

  • Penrod JT, Roth JR (2006) Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. J Bacteriol 188:2865–2874

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Price GD (2011) Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth Res 109:47–57

    Article  CAS  PubMed  Google Scholar 

  • Price GD, Badger MR (1991) Evidence for the role of carboxysomes in the cyanobacterial CO2-concentrating mechanism. Can J Bot 69:963–973

    Article  CAS  Google Scholar 

  • Price GD, Howitt SM, Harrison K, Badger MR (1993) Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. J Bacteriol 175:2871–2879

    CAS  PubMed Central  PubMed  Google Scholar 

  • Roberts EW, Cai F, Kerfeld CA, Cannon GC, Heinhorst S (2012) Isolation and characterization of the Prochlorococcus carboxysome reveal the presence of the novel shell protein CsoS1D. J Bacteriol 194:787–795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sagermann M, Ohtaki A, Nikolakakis K (2009) Crystal structure of the EutL shell protein of the ethanolamine ammonia lyase microcompartment. Proc Natl Acad Sci U S A 106:8883–8887

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samborska B, Kimber MS (2012) A dodecameric CcmK2 structure suggests β-carboxysomal shell facets have a double-layered organization. Structure 20:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Sawaya MR, Cannon GC, Heinhorst S, Tanaka S, Williams EB, Yeates TO, Kerfeld CA (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

    Article  CAS  PubMed  Google Scholar 

  • Schmid MF, Paredes AM, Khant HA, Soyer F, Aldrich HC, Chiu W, Shively JM (2006) Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography. J Mol Biol 364:526–535

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • So AK, Espie GS (1998) Cloning, characterization and expression of carbonic anhydrase from the cyanobacterium Synechocystis PCC6803. Plant Mol Biol 37:205–215

    Article  CAS  PubMed  Google Scholar 

  • So AK, Cot SS-W, Espie GS (2002) Characterization of the C-terminal extension of carboxysomal carbonic anhydrase from Synechocystis sp. PCC6803. Funct Plant Biol 29:183–194

    Article  CAS  Google Scholar 

  • So AK, Espie GS (2005) Cyanobacterial carbonic anhydrases. Can J Bot 83:721–734

    Article  CAS  Google Scholar 

  • So AK, Espie GS, Williams EB, Shively JM, Heinhorst S, Cannon GC (2004) A Novel evolutionary lineage of carbonic anhydrase (ɛ class) is a component of the carboxysome shell. J Bacteriol 186:623

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S, Cannon GC, Yeates TO (2008) Atomic-level models of the bacterial carboxysome shell. Science 319:1083–1086

    Article  CAS  PubMed  Google Scholar 

  • Tanaka S, Sawaya MR, Phillips M, Yeates TO (2009) Insights from multiple structures of the shell proteins from the beta-carboxysome. Protein Sci 18:108–120

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsai Y, Sawaya MR, Cannon GC, Cai F, Williams EB, Heinhorst S, Kerfeld CA, Yeates TO (2007) Structural analysis of CsoS1A and the protein shell of the Halothiobacillus neapolitanus carboxysome. PLoS Biol 5:e144

    Article  PubMed Central  PubMed  Google Scholar 

  • Tsai Y, Sawaya MR, Yeates TO (2009) Analysis of lattice-translocation disorder in the layered hexagonal structure of carboxysome shell protein CsoS1C. Acta Crystallogr D Biol Crystallogr 65:980–988

    Article  CAS  PubMed  Google Scholar 

  • Yeates TO, Crowley CS, Tanaka S (2010) Bacterial microcompartment organelles: protein shell structure and evolution. Annu Rev Biophys 39:185–205

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu JW, Price GD, Song L, Badger MR (1992) Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100:794–800

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by a Discovery Grant from the National Science and Engineering Research Council of Canada to MSK (# 327280).

Author information

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Matthew S. Kimber

Authors
  1. Matthew S. Kimber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew S. Kimber .

Editor information

Editors and Affiliations

  1. Department of Biotechnology, Norwegian University of Science and Technology, Trondheim, Sør-Trøndelag Fylke, Norway

    Martin F. Hohmann-Marriott

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Kimber, M.S. (2014). Carboxysomes – Sequestering RubisCO for Efficient Carbon Fixation. In: Hohmann-Marriott, M. (eds) The Structural Basis of Biological Energy Generation. Advances in Photosynthesis and Respiration, vol 39. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8742-0_7

Download citation

Publish with us

Policies and ethics

Search

Navigation