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Protein-based organelles in bacteria: carboxysomes and related microcompartments

Key Points

  • The complexity of bacterial cells is discussed, together with an explanation of the advantages that can be provided by an organelle that sequesters related enzymes in a pathway. The carboxysome is introduced as a bacterial microcompartment that functions to enhance CO2 fixation.

  • The discovery and early characterization of the carboxysome is discussed. Evidence for the function of the carboxysome is reviewed, together with the first isolation and purification of carboxysomes and identification of the proteins that constitute the shell.

  • The two types of carboxysome (α and β) are introduced. The important role of carbonic anhydrase is discussed, together with experiments that identify which genes encode carbonic anhydrase in the two types of carboxysome.

  • The main shell proteins and their genes are introduced for the two types of carboxysome. Other proteins that are associated with the shell are also introduced, most of which are not yet fully understood.

  • A discussion of the main shell protein from the carboxysome, which belongs to a family of proteins (the bacterial microcompartment domain family) that is widespread among bacteria is provided. Diverse microcompartments exist, with presumably similar shells, but distinct metabolic enzymes are encapsulated inside particular microcompartments. The list of organisms with microcompartments includes Escherichia coli and serovars of Salmonella enterica.

  • Recent structural studies on the carboxysome are highlighted. These include moderate-resolution reconstructions on the basis of cryo-electron tomography and high-resolution crystal structures of several shell proteins. The emerging principles of assembly and transport across the shell are presented.

  • Outstanding questions and future studies are indicated, the role of structure-guided mutagenesis is noted and the long-term goal of numerically modelling the behaviour of microcompartments is suggested, together with the long-term prospect for protein-engineering studies.

Abstract

Many bacteria contain intracellular microcompartments with outer shells that are composed of thousands of protein subunits and interiors that are filled with functionally related enzymes. These microcompartments serve as organelles by sequestering specific metabolic pathways in bacterial cells. The carboxysome, a prototypical bacterial microcompartment that is found in cyanobacteria and some chemoautotrophs, encapsulates ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase, and thereby enhances carbon fixation by elevating the levels of CO2 in the vicinity of RuBisCO. Evolutionarily related, but functionally distinct, microcompartments are present in diverse bacteria. Although bacterial microcompartments were first observed more than 40 years ago, a detailed understanding of how they function is only now beginning to emerge.

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Figure 1: Carboxysomes and the Pdu microcompartment.
Figure 2: The genes and genomic organization of carboxysomes and related bacterial microcompartments.
Figure 3: High-resolution structures of carboxysome shell proteins.

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Acknowledgements

The authors thank S. Tanaka for figure preparation and T. Bobik for discussions. T.O.Y. and C.A.K. have been supported by grants from the BER programme of the Department of Energy Office of Science and the US Department of Agriculture, G.C.C. and S.H. have been supported by the National Science Foundation (grant numbers MCB-0444568 and DMR-0213883, repectively) and G.C.C. and S.H. have been supported by the T.W. Bennett Foundation at The University of Southern Mississippi.

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DATABASES

Entrez Genome Project

Escherichia coli

Nitrobacter winogradskyi

Nitrococcus mobilis

Nostoc punctiforme

Prochlorococcus marinus str. MIT 9313

Prochlorococcus marinus subsp. pastoris str. CCMP1986

Rhodopseudomonas palustris BisB18

Salmonella enterica serovar Typhimurium

Synechococcus elongatus PCC 7942

Synechocystis sp. PCC 6803

Synechococcus sp. WH 8102

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Glossary

Bacterial microcompartment

A large, polyhedral, proteinaceous structure that functions as an organelle by encapsulating specific enzymes inside a protein shell that is reminiscent of a viral capsid.

Carboxysome

A polyhedral bacterial microcompartment that enhances carbon fixation by encapsulating the ribulose-1,5-bisphosphate carboxylase/oxygenase and carbonic anhydrase enzymes.

CO2 fixation

The process by which carbon in the biosphere is converted from an inorganic form (for example, CO2) into organic molecules.

Ribulose-1,5-bisphosphate carboxylase/oxygenase

The enzyme that fixes carbon by combining CO2 with the five-carbon compound ribulose-1,5-bisphosphate to form two molecules of the three-carbon compound phosphoglycerate.

Carbonic anhydrase

An enzyme that catalyses the interconversion of bicarbonate and CO2.

Icosahedron

A regular geometric solid that has 20 triangular faces and 12 vertices; a large icosahedron can be constructed by assembling hexagons together on the triangular faces with pentagons at the 12 vertices.

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Yeates, T., Kerfeld, C., Heinhorst, S. et al. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 6, 681–691 (2008). https://doi.org/10.1038/nrmicro1913

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