Bacterial microcompartments (BMCs) are organelles that segregate segments of metabolic pathways that are incompatible with the surrounding metabolism. These metabolic modules consist entirely of protein, thus they are directly genetically encoded organelles. The BMC membrane is composed of families of proteins that oligomerize into pentagonal and hexagonal building blocks, typically perforated by pores, that tile into a polyhedral shell. The shell protein families are structurally homologous, with the function of the BMC determined by the encapsulated enzymes and the permeability properties of the constituent shell proteins. BMCs can be identified bioinformatically by locating genes encoding shell proteins, which are generally found proximal to those for the encapsulated enzymes. We here performed a large-scale sequence-based analysis of all shell proteins across the bacterial tree of life. With recent advances in genome-resolved metagenomics and the emphasis on “microbial dark matter”, many new genome sequences from diverse and obscure bacterial species clades have become available. We find that locus-specific designations of shell proteins should be supplanted, because higher level patterns of co-occurrence are evident. Moreover, the number of identifiable BMC loci has increased twenty-fold since the last comprehensive census of 2014. While we can assign many to bioinformatically characterized loci, the addition of new types uncovered in this study doubles the number of distinct BMC types described. In addition, we predict several new functional types that expand the range of catalysis encapsulated in BMCs, an intriguing example is an organelle for the degradation of an aromatic substrate, compartmentalized in an unusually simple shell, with potential for bioremediation. Our comprehensive survey of bacterial metabolic organelles underscores that there is compartmentalized dark biochemistry yet to be discovered through genome sequencing. The finding of up to six distinct BMC loci in a single genome underscores the role of BMCs in conferring metabolic flexibility and provides new insights into how certain clades have adapted to or even dominate, as in dysbiosis, an environmental niche. Our catalog provides a rich substrate for downstream experimental characterization of these metabolic modules and broadens the foundation for the development of BMC-based nanoarchitectures for biomedical and bioengineering applications.
The purification and characterization of the peripheral antenna and the preliminary characterization of a carotenoid-protein complex from the purple-sulfur bacterium Chromatium purpuratum are described. The peripheral antenna of C. purpuratum is unusual among purple bacteria in that it can be resolved by SDS-PAGE into six subunits, the largest number observed thus far for a spectrally pure antenna complex. N-terminal sequence analyses of these subunits suggest that they may have an additional bacteriochlorophyll-binding site located outside the transmembrane domain. The results of pigment-protein quantification are also consistent with additional pigment-binding sites in the C. purpuratum LH2. Furthermore, CD measurements and sequence analysis suggest the presence of considerable beta-type in addition to alpha-helical secondary structure. Thus, the secondary and quaternary structures of this complex differ significantly from light-harvesting complexes of other purple photosynthetic bacteria. A carotenoid-protein complex is also described; it is an apparent association of three proteins and carotenoid and is closely associated with the peripheral antenna. The purple-sulfur bacteria are evolutionarily older than the relatively better characterized purple-nonsulfur organisms. The phenotypic features described here of the C. purpuratum photosynthetic apparatus are related to those of other purple bacteria and green-sulfur bacteria and may reflect the evolutionary position of this organism.
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