Diverse Bacterial Microcompartment Organelles

Abstract

SUMMARY Bacterial microcompartments (MCPs) are sophisticated protein-based organelles used to optimize metabolic pathways. They consist of metabolic enzymes encapsulated within a protein shell, which creates an ideal environment for catalysis and facilitates the channeling of toxic/volatile intermediates to downstream enzymes. The metabolic processes that require MCPs are diverse and widely distributed and play important roles in global carbon fixation and bacterial pathogenesis. The protein shells of MCPs are thought to selectively control the movement of enzyme cofactors, substrates, and products (including toxic or volatile intermediates) between the MCP interior and the cytoplasm of the cell using both passive electrostatic/steric and dynamic gated mechanisms. Evidence suggests that specialized shell proteins conduct electrons between the cytoplasm and the lumen of the MCP and/or help rebuild damaged iron-sulfur centers in the encapsulated enzymes. The MCP shell is elaborated through a family of small proteins whose structural core is known as a bacterial microcompartment (BMC) domain. BMC domain proteins oligomerize into flat, hexagonally shaped tiles, which assemble into extended protein sheets that form the facets of the shell. Shape complementarity along the edges allows different types of BMC domain proteins to form mixed sheets, while sequence variation provides functional diversification. Recent studies have also revealed targeting sequences that mediate protein encapsulation within MCPs, scaffolding proteins that organize lumen enzymes and the use of private cofactor pools (NAD/H and coenzyme A [HS-CoA]) to facilitate cofactor homeostasis. Although much remains to be learned, our growing understanding of MCPs is providing a basis for bioengineering of protein-based containers for the production of chemicals/pharmaceuticals and for use as molecular delivery vehicles.

In Salmonella enterica, Ethanolamine Utilization Is Repressed by 1,2-Propanediol To Prevent Detrimental Mixing of Components of Two Different Bacterial Microcompartments

“…Recent genomic analyses showed that nearly 40% of MCP-encoding species have genes for multiple MCP systems (1). Furthermore, the BMC domain proteins that form the shells of MCPs are homologous across the known types of MCP systems, including the Pdu, Eut, Grp, and carboxysome systems (5,6), and are understood to assemble via conserved edge complementarity. Given the widespread homology of MCP shell proteins and the BMC domain present in these proteins, it is likely that a myriad of other bacterial species which have the capacity to express multiple MCP systems (1) also have some mechanism to regulate proper assembly and function of these MCPs.…”

“…(19,20). The metabolic pathways, structure, and regulation of these MCPs have been the subject of a number of studies (5).The Pdu MCP consists of a protein shell that encapsulates 1,2-PD-degradative enzymes, and its function is to sequester a pathway intermediate (propionaldehyde) that is toxic and poorly retained by the cell envelope (19,(21)(22)(23). Production of Pdu MCPs is under the control of the regulatory protein PocR, and they are induced in the presence of 1,2-PD (24,25).…”

“…MCPs consist of metabolic enzymes encapsulated within a protein shell, and their function is to optimize certain metabolic pathways by confining toxic and/or volatile metabolic intermediates (5,6). Confinement helps to prevent carbon loss, increases metabolic flux, and mitigates cellular toxicity.…”

“…The best-studied MCPs are the carboxysomes of cyanobacteria and chemoautotrophs, which are used to enhance autotrophic CO 2 fixation via the Calvin cycle (6). Two other wellstudied MCPs are used to optimize growth on 1,2-propanediol (1,2-PD) or ethanolamine (Pdu and Eut MCPs) (5). Both 1,2-PD and ethanolamine are important carbon sources in anaerobic environments, and the ability to degrade these compounds is thought to provide a competitive advantage to enteric pathogens, such as Salmonella, in the inflamed intestine (7)(8)(9)(10).…”

Ethanolamine Catabolism in Pseudomonas aeruginosa PAO1 Is Regulated by the Enhancer-Binding Protein EatR (PA4021) and the Alternative Sigma Factor RpoN

“…In addition to this set of core enzymes, some bacteria possess several other auxiliary proteins that aid in the catabolism of ethanolamine (11). For example, members of the Enterobacteriaceae often utilize an alcohol dehydrogenase (EutG) that reduces acetaldehyde to ethanol and shell proteins (EutSMNLK), which form a microcompartment to encapsulate the ethanolamine-degrading enzymes (10,(12)(13)(14).…”