Abstract
Bacterial microcompartments (BMCs) are proteinaceous organelles involved in both autotrophic and heterotrophic metabolism. All BMCs share homologous shell proteins but differ in their complement of enzymes; these are typically encoded adjacent to shell protein genes in genetic loci, or operons. To enable the identification and prediction of functional (sub)types of BMCs, we developed LoClass, an algorithm that finds putative BMC loci and inventories, weights, and compares their constituent pfam domains to construct a locus similarity network and predict locus (sub)types. In addition to using LoClass to analyze sequences in the Non-redundant Protein Database, we compared predicted BMC loci found in seven candidate bacterial phyla (six from single-cell genomic studies) to the LoClass taxonomy. Together, these analyses resulted in the identification of 23 different types of BMCs encoded in 30 distinct locus (sub)types found in 23 bacterial phyla. These include the two carboxysome types and a divergent set of metabolosomes, BMCs that share a common catalytic core and process distinct substrates via specific signature enzymes. Furthermore, many Candidate BMCs were found that lack one or more core metabolosome components, including one that is predicted to represent an entirely new paradigm for BMC-associated metabolism, joining the carboxysome and metabolosome. By placing these results in a phylogenetic context, we provide a framework for understanding the horizontal transfer of these loci, a starting point for studies aimed at understanding the evolution of BMCs. This comprehensive taxonomy of BMC loci, based on their constituent protein domains, foregrounds the functional diversity of BMCs and provides a reference for interpreting the role of BMC gene clusters encoded in isolate, single cell, and metagenomic data. Many loci encode ancillary functions such as transporters or genes for cofactor assembly; this expanded vocabulary of BMC-related functions should be useful for design of genetic modules for introducing BMCs in bioengineering applications.
Highlights
Membrane-bound organelles for compartmentalization of specific functions are the hallmark feature of all eukaryotic cells
Our results provide the first glimpse of the extent of Bacterial microcompartments (BMCs) metabolic diversity and will inform design of genetic modules encoding BMCs for introduction of new metabolic functions in a plug-and-play approach
Analysis of Loci from Candidate Phyla In order to identify BMC loci in genomes from candidate phyla not archived in Non-redundant Protein Database (NR), we examined the single-cell genomes from the recent GEBA-MDM project [52] for the presence of BMC shell protein genes using the Integrated Microbial Genomes (IMG) Database [53]
Summary
Membrane-bound organelles for compartmentalization of specific functions are the hallmark feature of all eukaryotic cells. Anammoxosomes are lipid-bound compartments that enable certain planctomycetes to obtain energy from anaerobic ammonium oxidation (reviewed in [1]), and magnetosomes are invaginations of the inner membrane that allow magnetotactic bacteria to orient along the Earth’s magnetic field to search for microaerobic environments (reviewed in [2]). Another type of organelle, composed entirely of protein, is the bacterial microcompartment (BMC) (reviewed in [3,4,5]). Several studies have shown that all three components are required for the construction of fully functional carboxysomes [16,17,18]
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