Bacterial microcompartment
[3][5][7][13][14] Other protein-based compartments found in bacteria and archaea include encapsulin nanocompartments[15] and big gas vesicles.
[16] The first BMCs were observed in the 1950s in electron micrographs of cyanobacteria,[17] and were later named carboxysomes after their role in carbon fixation was established.
Subsequently, transmission electron micrographs of Salmonella cells grown on propanediol[21] or ethanolamine[22] showed the presence of polyhedral bodies similar to carboxysomes.
Most of the genes (coding for the shell proteins and the encapsulated enzymes) from experimentally characterized BMCs are located near one another in distinct genetic loci or operons.
[24] In 2021, in an analysis of over 40,000 shell protein sequences, it was shown that at least 45 phyla have members that encode BMCs,[2] and the number of functional types and subtypes has increased to 68.
Collectively, these structures shown that the basic principles of shell assembly are universally conserved across functionally distinct BMCs.
[27] The crystal structures of a number of these proteins have been determined, showing that they assemble into cyclical hexamers, typically with a small pore in the center.
Most BMCs contain multiple distinct types of BMC-H proteins (paralogs) that tile together to form the facets, likely reflecting the range of metabolites that must enter and exit the shell.
In such structures, one pore from one trimer is in an “open” conformation, while the other is closed – suggesting that there may be an airlock-like mechanism that modulates the permeability of some BMC shells.
[50][51] Similarly, for the PDU BMC, the shell must be permeable to propanediol, propanol, propionyl-phosphate, and potentially also vitamin B12, but it is clear that propionaldehyde is somehow sequestered to prevent cell damage.
[3][5][14][53] In the PDU microcompartment, mutagenesis experiments have shown that the pore of the PduA shell protein is the route for entry of the propanediol substrate.
[32][35][55] In the EUT microcompartment, gating of the large pore in the EutL shell protein is regulated by the presence of the main metabolic substrate, ethanolamine.
[51][58] Mutants that lack genes coding for the carboxysome shell display a high CO2 requiring phenotype due to the loss of the concentration of carbon dioxide, resulting in increased oxygen fixation by RuBisCO.
[50] In addition to the anabolic carboxysomes, several catabolic BMCs have been characterized that participate in the heterotrophic metabolism via short-chain aldehydes; they are collectively termed metabolosomes.
Ethanol is likely a lost carbon source, but acetyl-phosphate can either generate ATP or be recycled to acetyl-CoA and enter the TCA cycle or several biosynthetic pathways.
[22] Some bacteria, especially those in the genus Listeria, encode a single locus in which genes for both PDU and EUT BMCs are present.
[69] One GRM locus in Clostridium phytofermentans has been shown to be involved in the fermentation of fucose and rhamnose, which are initially degraded to 1,2-propanediol under anaerobic conditions.
The glycyl radical enzyme is proposed to dehydrate propanediol to propionaldehyde, which is then processed in a manner identical to the canonical PDU BMC.
The aldehyde generated in this predicted pathway would be the extremely toxic compound methylglyoxal; its sequestration within the BMC could protect the cell.
[24] One type of BMC locus does not contain RuBisCO or any of the core metabolosome enzymes, and has been proposed to facilitate a third category of biochemical transformations (i.e. neither carbon fixation nor aldehyde oxidation).
[76] Some micrographs indicate that their assembly occurs as a simultaneous coalescence of enzymes and shell proteins as opposed to the seemingly stepwise fashion observed for beta-carboxysomes.
[73][83][84][85][86] With the exception of cyanobacterial carboxysomes, in all tested cases, BMCs are encoded in operons that are expressed only in the presence of their substrate.
[88] EUT BMCs in Salmonella enterica are induced via the regulatory protein EutR by the simultaneous presence of ethanolamine and vitamin B12, which can happen under aerobic or anaerobic conditions.
[90] PVM BMCs in Planctomyces limnophilus are induced by the presence of fucose or rhamnose under aerobic conditions, but not by glucose.
[77] Carboxysomes also provide an example of how knowledge of a BMC assembly pathway enables simplification and reduction in the number of necessary gene products for organelle construction.
[107] Additional technical advances, such as the ability to construct shells in vitro[108] are rapidly enabling the development of BMCs in biotechnology.
