Bacterial microcompartment organelles: protein shell structure and evolution - PubMed (original) (raw)

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Bacterial microcompartment organelles: protein shell structure and evolution

Todd O Yeates et al. Annu Rev Biophys. 2010.

Abstract

Some bacteria contain organelles or microcompartments consisting of a large virion-like protein shell encapsulating sequentially acting enzymes. These organized microcompartments serve to enhance or protect key metabolic pathways inside the cell. The variety of bacterial microcompartments provide diverse metabolic functions, ranging from CO(2) fixation to the degradation of small organic molecules. Yet they share an evolutionarily related shell, which is defined by a conserved protein domain that is widely distributed across the bacterial kingdom. Structural studies on a number of these bacterial microcompartment shell proteins are illuminating the architecture of the shell and highlighting its critical role in controlling molecular transport into and out of microcompartments. Current structural, evolutionary, and mechanistic ideas are discussed, along with genomic studies for exploring the function and diversity of this family of bacterial organelles.

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Figures

Figure 1

Figure 1. Electron micrographs of various bacterial microcompartments

(a) Transmission electron micrographs showing (left) a section through a dividing cyanobacterial cell (Synechocystis sp. PCC 6803) and (right) an enlargement of a single carboxysome on the right (courtesy of Wim Vermaas) (adapted from Reference 39). (b) Purified carboxysomes from Halothiobacillus neapolitanus (sample courtesy of Sabine Heinhorst and Gordon Cannon, image courtesy of Kelly Dryden and Mark Yeager). (c) Isolated Pdu microcompartments from Salmonella enterica serovar Typhimurium LT2 (courtesy of Thomas Bobik).

Figure 2

Figure 2

Gene organization and proposed metabolic pathways for three types of bacterial microcompartments. Genes are colored to indicate their homology. All BMC shell proteins are light blue. For each microcompartment, the key sequestered intermediate is boxed in orange. (a) Function of the carboxysome in enhancing CO2 fixation. See text and Reference for mechanistic details. Gene organizations for α- and β-carboxysomes are on the right. (b) A current model for the function of the propanediol utilization (Pdu) microcompartment in metabolizing 1,2-propanediol. See text and Reference for mechanistic details. The gene organization for the pdu operon is shown on the right. (c) A hypothetical model for the metabolism of ethanolamine in the Eut microcompartment. See text and Reference for mechanistic details. The gene organization of the eut operon is shown on the right.

Figure 3

Figure 3

Idealized model for assembly of the carboxysome and related bacterial microcompartments. (a) A ribbon diagram of a typical bacterial microcompartment (BMC) shell protein fold. (b) A hexameric assembly of a BMC protein in a ribbon diagram. (c) Hexameric building blocks of the BMC proteins can assemble into a molecular layer (right), which forms flat facets of the polyhedral shells of various bacterial microcompartments. The pentameric proteins (CcmL or CsoS4A) from the carboxysome (bottom, right) have been argued to form vertices of the icosahedral carboxysome (left) (68). The Pdu and Eut microcompartments are less geometrically regular than the carboxysome and are potentially more complex.

Figure 4

Figure 4

Sequence conservation among diverse bacterial microcompartment (BMC) shell proteins. Conserved amino acid positions (red) were defined as those having sequence identity above 80% in an alignment of 2174 BMC sequences. Positions of high conservation occur mainly at the perimeter, where hexamers meet. In the CcmK1 protein, these residues include A4, G6, A19, D21, K25, V29, G38, G48, V50, V53, and G70; the conserved residue in the pore is glycine G38.

Figure 5

Figure 5

Variations on the bacterial microcompartment (BMC) protein fold. (Top) Secondary structure schematics of BMC proteins in their various arrangements. Individual secondary structure elements are colored. The canonical BMCs include CcmK1/2/3/4, CsoS1A/B/C, PduA/J, and EutM. CcmO likely encodes tandem canonical BMC domains. The permuted, single-domain BMC proteins include PduU and EutS. (Bottom, right) The cores of canonical and permuted BMC proteins are in close agreement, as shown by a superposition of PduU (salmon) over CcmK2 (yellow). (Bottom, left) Both EutL and CsoS1D have permuted BMC domains in tandem, but their tertiary arrangements differ. Individual BMC domains are colored separately. When the N-terminal BMC domains (blue) of the two proteins are superimposed, their C-terminal domains (CsoS1D in magenta and EutL in green) adopt different positions in the hexamer. The linker regions between domains are colored yellow.

Figure 6

Figure 6

Various pores of bacterial microcompartment (BMC) proteins. Top views of central pores from some representative BMC proteins colored by electrostatic potential (positive: blue; negative: red). Canonical BMC proteins (e.g., CcmK1 from the β-carboxysome) have a small pore at the sixfold, which has a diameter of 4 to 6 Å (39, 69, 72). A circularly permutated tandem BMC protein from the α-carboxysome, CsoS1D, adopts alternative conformations with open and closed pores (40). A circularly permutated BMC protein from the pdu microcompartment, PduU, revealed a totally closed pore (19). Whether this pore opens for transport is unknown. Another circularly permutated tandem BMC protein, EutL, has been observed in two distinct conformations, open (70) (not shown) and closed (40, 70) (shown). See Supplemental Figure 2 for additional views of the pores.

Figure 7

Figure 7

Schematic for identifying conserved bacterial microcompartment (BMC)-proximal protein families. First, BMC homologues were retrieved from the NCBI database (CDD ID cl01982). Their respective chromosomal positions were located in fully sequenced bacterial genomes deposited into the EBI Integr8 database. For each chromosomal position identified, 10 BMC-proximal open reading frames in both the 5′ and 3′ direction were retrieved as candidate microcompartment-associated genes and subsequently assigned to homologous sequence clusters by performing a full pairwise BLAST analysis. The dominant clusters suggest likely microcompartment-associated functions (Supplemental Tables 2 and 3).

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