Carboxysomes and Their Structural Organization in Prokaryotes
Carboxysomes are the archetypical examples of primitive proteinaceous organelles found in bacteria, collectively termed bacterial microcompartments (BMCs). Recent studies using current techniques for imaging and structural elucidation have resulted in a quantum leap of our mechanistic understanding of structure/function relationships in these bacterial inclusions. Bioinformatic analysis of the rapidly growing collection of sequenced bacterial genomes has revealed that BMCs of different types appear to be widely employed by microbes to organize their metabolism in much the same way that eukaryotes use sensu stricto organelles. This review focuses on some recently revealed properties of carboxysomes and points out pressing open questions. Some of these questions have remained unanswered since the discovery of carboxysomes; others have been raised by more recent discoveries.
KeywordsPermeability Codon Polypeptide Bicarbonate Disulfide
The authors are grateful to Drs. Fei Cai, Cheryl Kerfeld, Cristina Iancu, and Grant Jensen for the images they provided and their help with various figures in this review. We truly appreciate the many stimulating discussions we have had throughout the years of our respective collaborations. SH and GCC acknowledge the generous funding of their carboxysome research from the National Science Foundation (current awards: MCB-0851070 and MCB-1244534).
- Beudeker RF, Cannon GC, Kuenen JG, Shively JM (1980) Relations between d-ribulose-1,5-bisphosphate carboxylase, carboxysomes, and CO2 fixing capacity in the obligate chemolithotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. Arch Microbiol 124:185–189CrossRefGoogle Scholar
- Heinhorst S, Cannon GC, Shively JM (2006) Carboxysomes and carboxysome-like inclusions. In: Shively JM (ed) Complex intracellular structures in prokaryotes, vol 2. Springer, Berlin, pp 141–164Google Scholar
- Jensen TE (1984) Cyanobacterial cell inclusions of irregular occurrence: systematic and evolutionary implications. Cytobios 39:35–62Google Scholar
- Menon BB, Dou Z, Milam J, Shively JM, Heinhorst S, Cannon GC (2009) Phenotypic analysis of a Halothiobacillus neapolitanus mutant harboring beta-cyanobacterial form IB RubisCO. In: Amercian society for microbiology 109th general meeting Philadelphia, PA. K–066Google Scholar
- Orus MI, Rodriguez-Buey ML, Marco E, Fernandez-Valiente E (2001) Changes in carboxysome structure and grouping and in photosynthetic affinity for inorganic carbon in Anabaena strain PCC 7119 (Cyanophyta) in response to modification of CO2 and Na+ supply. Plant Cell Physiol 42:46–53PubMedCrossRefGoogle Scholar
- Peters K-R (1974) Characterisierung eines phagenaehnlichen Partikels aus Zellen von Nitrobacter. Arch Microbiol 97:129–140Google Scholar
- Price GD, Badger MR (1989) Isolation and characterization of high CO2-requiring-mutants of the cyanobacterium Synechococcus PCC 7942: two phenotypes that accumulate inorganic carbon but are apparently unable to generate CO2 within the carboxysome. Plant Physiol 91:514–525PubMedCentralPubMedCrossRefGoogle Scholar
- Price GD, Sültemeyer D, Klughammer B, Ludwig M, Badger MR (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins and recent advances. Can J Bot 76:973–1002Google Scholar
- Reinhold L, Zviman M, Kaplan A (1989) A quantitative model for carbon fluxes and photosynthesis in cyanobacteria. Plant Physiol Biochem 27:945–954Google Scholar
- Shively JM, Ball FL, Kline BW (1973b) Electron microscopy of the carboxysomes (polyhedral bodies) of Thiobacillus neapolitanus. J Bacteriol 116:1405–1411Google Scholar
- Tang M, Jensen TE, Corpe WA (1995) The occurrence of polyphosphate bodies in polyhedral bodies (carboxysomes) in Synechococcus leopoliensis (Cyanophyceae). Microbios 81:59–66Google Scholar