Assembly, function and evolution of cyanobacterial carboxysomes
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Section snippets
Introduction: carboxysomes: metabolic modules for CO2 fixation
More than 50 years ago, unusual polyhedral bodies were discovered in cyanobacteria by electron microscopy [1] (Figure 1a–c). They were subsequently identified as proteinaceous shells that were packed with the CO2-fixation enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and, accordingly, named carboxysomes [2]. Through identification of homologs of the delimiting shell proteins in microbial genomes, it is now known that carboxysomes are members of a class of
Alpha and beta carboxysomes are distinct BMCs
Although alpha and beta carboxysomes share similar general architectural and functional principles — a selectively permeable protein shell that encapsulates RuBisCO with CA — they differ in many details, including the type of RuBisCO (Form 1A in alpha, Form 1B in beta). The ‘core’ operons (Table 1) for alpha (cso) and beta (ccm) carboxysomes differ in the type of carbonic anhydrase encapsulated (CsoSCA, a beta-class CA; CcmM, a gamma-class CA). In addition to CcmM, a subset of cyanobacterial
Assembly of alpha and beta carboxysomes
The distinctive structural components of the alpha and beta carboxysomes are likely related to fundamental differences in their modes of assembly (Figure 2). Cryo-electron tomography studies on Halothiobacillus neapolitanus, the chemoautotrophic model organism for alpha carboxysome research [26], revealed partially assembled shells with attached RuBisCO molecules [27••], suggesting a co-assembly pathway for shell and cargo proteins. Indeed some of the internal, core proteins appear to be
Evolution of carboxysomes
For large multiprotein complexes, assembly pathways frequently reflect their evolution [39, 40]. Given the similarities among the structural features that are essential for assembly [4], we suggest that beta carboxysomes are more closely related to the metabolosomes (heterotrophic BMCs) than to the alpha carboxysomes. This inference is supported by a phylogenetic analysis of all BMC-P shell protein sequences (Figure 3). The alpha cyanobacterial sequences (for both the conserved CsoS4A and
Prospects
BMCs can be considered units of evolution, with their broad species distribution, conserved locus structure, and considerable evidence for their frequent horizontal gene transfer [3••, 4, 5]. These features likewise are establishing BMC loci as units of engineering, when viewed as genetically-encoded metabolic modules which can be transferred for plug-and-play applications in synthetic biology [4, 53]. For example, the canonical cso operon for the alpha carboxysome has been expressed in E. coli
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We thank members of the Kerfeld lab for engaging discussions, Dr. C. Raul Gonzalez for electron micrographs of cyanobacteria, and Dr. Fei Cai for micrographs of purified carboxysome shells and for a critical reading and assistance in revising this manuscript. This work was supported by the Office of Science of the U.S. Department of Energy DE-FG02-91ER20021 and with infrastructure support from MSU AgBio Research.
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