Prokaryotic Organelles: Bacterial Microcompartments in E. coli and Salmonella

Abstract

Bacterial microcompartments (MCPs) are proteinaceous organelles consisting of a metabolic pathway encapsulated within a selectively permeable protein shell. Hundreds of species of bacteria produce MCPs of at least nine different types, and MCP metabolism is associated with enteric pathogenesis, cancer, and heart disease. This review focuses chiefly on the four types of catabolic MCPs (metabolosomes) found in Escherichia coli and Salmonella: the propanediol utilization (pdu), ethanolamine utilization (eut), choline utilization (cut), and glycyl radical propanediol (grp) MCPs. Although the great majority of work done on catabolic MCPs has been carried out with Salmonella and E. coli, research outside the group is mentioned where necessary for a comprehensive understanding. Salient characteristics found across MCPs are discussed, including enzymatic reactions and shell composition, with particular attention paid to key differences between classes of MCPs. We also highlight relevant research on the dynamic processes of MCP assembly, protein targeting, and the mechanisms that underlie selective permeability. Lastly, we discuss emerging biotechnology applications based on MCP principles and point out challenges, unanswered questions, and future directions.

Figure 1

A comparison of selected MCP operons. Representative operons from S. enterica LT2 (pdu, eut), E. coli 536 (cut), and E. coli CFT073 (grp) are shown using one-letter abbreviations for genes and protein products. Gene sizes and spacing are roughly to scale. Note that in the cut operon, shell proteins are named with a different acronym, CmcA to -E to avoid redundancy with prior work.

Figure 2

Schematic of MCP pathways discussed in the text. (A) Pdu MCP; (B) Eut MCP; (C) Cut MCP; (D) Grp MCP. Shell protein names are shown in brown, signature enzymes in green, accessory enzymes (where applicable) in light green, aldehyde dehydrogenase in purple, alcohol dehydrogenase in red, phosphotransacetylase in blue, and acetate kinase in gold.

Figure 3

Electron micrographs of bacteria expressing MCPs, indicated by arrows. (A) Cut MCPs from E. coli 536; (B) Grp MCPs from E. Coli CFT073; (C) Pdu MCPs from S. enterica. Scale bars are located on each image. Images were obtained as described (76).

Figure 4

Representative crystal structures of select MCP shell proteins. (A) PduA BMC-H protein from S. enterica typhimurium (PDB ID: 3NGK) (155); (B) EutM, the orthologous BMC-H protein from E. coli K-12 (3I6P) (159); (C) PduU permuted BMC-H protein from S. enterica serovar Typhimurium (3CGI) (154); (D) EutL BMC-T closed form from E. coli K12 (3GFH) (160); (E) EutL BMC-T open form from E. coli K12 (3I87) (159); (F) PduT [Fe-S]-containing BMC-T protein from C. freundii (3PAC) [156]; (G) GrpN BMV pentamer from R. rubrum (4I7A) (158).