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Bacterial microcompartments

Key Points

  • Bacterial microcompartments are functional analogues of the lipid-bound organelles of eukaryotes. They enclose chemical reactions that benefit from being separated from the cytosol.

  • The delimiting membrane of bacterial microcompartments consists entirely of protein, and its components are highly conserved in sequence and structure.

  • Bacterial microcompartments are found in a wide variety of bacterial species (at least 19 established phyla). They are easily identified in genomes by their tendency to colocalize the associated genes into a large gene cluster called a superlocus.

  • Carboxysomes (CO2-fixing organelles) were the first type of bacterial microcompartment to be identified, but recently, many more have been discovered and characterized; they are involved in catabolizing a variety of nutrients and enable cells to grow in otherwise unavailable niches.

  • The shell and cargo of bacterial microcompartments self-assemble using different pathways; some build the shell around a cargo aggregate, whereas others assemble the shell and cargo concomitantly. There are proteins that facilitate cargo aggregation and small encapsulation peptides that specifically associate proteins to the lumen of the shell.

  • Bacterial microcompartments are linked to the pathogenesis of certain bacteria because they confer a growth advantage. For example, the human gut is enriched in propanediol and ethanolamine, initial substrates of specific bacterial microcompartments.

  • The knowledge gained from understanding the native functions has led to substantial progress in modifying the shell for bioengineering purposes. Bacterial microcompartment shells can be produced recombinantly, and shell proteins and cores have been engineered to adopt new functions.

Abstract

Bacterial microcompartments (BMCs) are self-assembling organelles that consist of an enzymatic core that is encapsulated by a selectively permeable protein shell. The potential to form BMCs is widespread and found across the kingdom Bacteria. BMCs have crucial roles in carbon dioxide fixation in autotrophs and the catabolism of organic substrates in heterotrophs. They contribute to the metabolic versatility of bacteria, providing a competitive advantage in specific environmental niches. Although BMCs were first visualized more than 60 years ago, it is mainly in the past decade that progress has been made in understanding their metabolic diversity and the structural basis of their assembly and function. This progress has not only heightened our understanding of their role in microbial metabolism but is also beginning to enable their use in a variety of applications in synthetic biology. In this Review, we focus on recent insights into the structure, assembly, diversity and function of BMCs.

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Figure 1: Core biochemistry of carboxysomes and metabolosomes and superloci organization.
Figure 2: Overview of bacterial microcompartments in different phyla and tree of shell pentamers.
Figure 3: Schematics of bacterial microcompartment structure.
Figure 4: Schematics of bacterial microcompartment assembly pathways.
Figure 5: Example of strategies to design synthetic bio-nanoreactors and scaffolding architectures using building blocks from bacterial microcompartments.
Figure 6: Timeline of research on bacterial microcompartments.

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Acknowledgements

This work was supported by the National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID) grant 1R01AI114975-01 with infrastructure support from the U.S. Department of Energy, Basic Energy Sciences, Contract DE-FG02-91ER20021.

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C.A.K., C.A., J.Z., F.C. and M.S. contributed to researching data for the article. C.A.K., C.A., J.Z., F.C. and M.S. substantially contributed to the discussion of content. C.A.K. and M.S. wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Cheryl A. Kerfeld.

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PowerPoint slides

Glossary

Carbonic anhydrase

An enzyme that catalyses the conversion of bicarbonate to carbon dioxide (and vice versa); the several subclasses of carbonic anhydrases have distinct structural folds.

Rubisco

An enzyme that fixes carbon dioxide by reacting it with ribulose-1,5-bisphosphate to create two molecules of phosphoglycerate. Form 1 Rubisco is composed of eight small and eight large subunits.

Calvin–Benson–Bassham cycle

A pathway for producing phosphoglyceraldehyde from CO2.

Superloci

Regions on the chromosome that contain one or more operons encoding genes for a bacterial microcompartment and ancillary proteins that support the function of the organelle.

BMC-H

A type of shell protein containing a single Pfam00936 domain that forms cyclic homohexamers.

BMC-T

A shell protein that contains two Pfam00936 domains that form cyclic homodimers or pseudohexamers.

BMC-P

A type of protein containing the Pfam03319 domain that forms homopentamers and functions as the pentagonal vertices of the BMC shell.

Pfam00936 domain

An 90 amino acid sequence that folds into an α-β structure that oligomerizes into a hexamer.

Facets

Surfaces connecting the icosahedral vertices.

α-Carboxysomes

One of two types of carboxysome; α-carboxysomes encapsulate form 1A Rubisco and are found primarily in marine cyanobacteria and chemoautotrophs.

β-Carboxysomes

This type of carboxysome is found in ecophysiologically diverse cyanobacteria; it encapsulates form 1B Rubisco, the form found in higher plants.

γ-Carbonic anhydrase

A subclass of carbonic anhydrases with a characteristic structure of three chains that each form a left-handed β-helix and a metal ion active site.

Encapsulation peptide

One or more short (17 amino acid) amphipathic helices that target cargo proteins to the interior of bacterial microcompartments; they are typically located at the N-terminus or C-terminus of a protein and are connected by an unstructured linker.

Glycyl radical enzymes

(GREs). A class of enzymes that uses radicals of glycine and cysteine for catalysis; they are highly oxygen sensitive and require an activating enzyme containing an Fe–S cluster to generate the glycyl radical.

Signature enzyme

An enzyme of a metabolosome that is specific to the initial substrate of the bacterial microcompartment.

Maximum-likelihood tree

A phylogenetic tree constructed using a computationally intense method that searches for the tree that has the highest probability of producing the observed data.

Pathogenicity islands

Segments of chromosomes that encode virulence factors and are found in pathogenic microorganisms but absent in closely related, non-pathogenic strains.

Fe–S clusters

Metal clusters composed of non-haem iron and sulfur atoms; in proteins, they function to transfer electrons over a wide range of potentials.

Ferredoxins

A family of proteins that contain Fe–S clusters to mediate electron transfer.

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Kerfeld, C., Aussignargues, C., Zarzycki, J. et al. Bacterial microcompartments. Nat Rev Microbiol 16, 277–290 (2018). https://doi.org/10.1038/nrmicro.2018.10

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