A catalog of the diversity and ubiquity of bacterial microcompartments

AbstractBacterial microcompartments (BMCs) are organelles that segregate segments of metabolic pathways which are incompatible with surrounding metabolism. BMCs consist of a selectively permeable shell, composed of three types of structurally conserved proteins, together with sequestered enzymes that vary among functionally distinct BMCs. Genes encoding shell proteins are typically clustered with those for the encapsulated enzymes. Here, we report that the number of identifiable BMC loci has increased twenty-fold since the last comprehensive census of 2014, and the number of distinct BMC types has doubled. The new BMC types expand the range of compartmentalized catalysis and suggest that there is more BMC biochemistry yet to be discovered. Our comprehensive catalog of BMCs provides a framework for their identification, correlation with bacterial niche adaptation, experimental characterization, and development of BMC-based nanoarchitectures for biomedical and bioengineering applications.

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A Catalog of the Diversity and Ubiquity of Metabolic Organelles in Bacteria

10.1101/2021.01.25.427685 ◽

2021 ◽

Author(s):

Markus Sutter ◽

Matthew R. Melnicki ◽

Frederik Schulz ◽

Tanja Woyke ◽

Cheryl A. Kerfeld

Keyword(s):

Dark Matter ◽

Genome Sequencing ◽

Metabolic Pathways ◽

Experimental Characterization ◽

Genome Sequences ◽

Permeable Membrane ◽

Bacterial Microcompartments ◽

Niche Adaptation ◽

Genes Encoding ◽

Shell Proteins

AbstractBacterial microcompartments (BMCs) are organelles that segregate segments of metabolic pathways, which are incompatible with surrounding metabolism. In contrast to their eukaryotic counterparts, the selectively permeable membrane of BMCs, the shell, is composed of protein. While the sequestered enzymes vary among functionally distinct BMCs, the proteins that form diverse BMC shells are structurally homologous; this enables the bioinformatic identification of the organelles by locating genes encoding shell proteins, which are typically proximal to those for the encapsulated enzymes. With recent advances in genome‐resolved metagenomics and the emphasis on “microbial dark matter”, many new genome sequences from diverse and obscure bacterial clades have become available. We find the number of identifiable BMC loci has increased twenty‐fold since the last comprehensive census of 2014. Moreover, the addition of new types we uncovered doubles the number of distinct BMC types known. These expand the range of catalysis encapsulated in BMCs, underscoring that there is dark biochemistry that is compartmentalized in bacterial organelles yet to be discovered through genome sequencing. Our comprehensive catalog of BMCs provides a framework for their identification, correlation with bacterial niche adaptation, and experimental characterization, and broadens the foundation for the development of BMC‐based nanoarchitectures for biomedical and bioengineering applications.

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Clues to the function of bacterial microcompartments from ancillary genes

Biochemical Society Transactions ◽

10.1042/bst20200632 ◽

2021 ◽

Author(s):

Henning Kirst ◽

Cheryl A. Kerfeld

Keyword(s):

Metabolic Pathways ◽

Transmembrane Proteins ◽

Transcriptional Regulators ◽

Building Blocks ◽

Data Set ◽

Bacterial Phyla ◽

Bacterial Microcompartments ◽

Shell Proteins ◽

Regulation Mechanisms ◽

Protein Shell

Bacterial microcompartments (BMCs) are prokaryotic organelles. Their bounding membrane is a selectively permeable protein shell, encapsulating enzymes of specialized metabolic pathways. While the function of a BMC is dictated by the encapsulated enzymes which vary with the type of the BMC, the shell is formed by conserved protein building blocks. The genes necessary to form a BMC are typically organized in a locus; they encode the shell proteins, encapsulated enzymes as well as ancillary proteins that integrate the BMC function into the cell's metabolism. Among these are transcriptional regulators which usually found at the beginning or end of a locus, and transmembrane proteins that presumably function to conduct the BMC substrate into the cell. Here, we describe the types of transcriptional regulators and permeases found in association with BMC loci, using a recently collected data set of more than 7000 BMC loci distributed over 45 bacterial phyla, including newly discovered BMC loci. We summarize the known BMC regulation mechanisms, and highlight how much remains to be uncovered. We also show how analysis of these ancillary proteins can inform hypotheses about BMC function; by examining the ligand-binding domain of the regulator and the transporter, we propose that nucleotides are the likely substrate for an enigmatic uncharacterized BMC of unknown function.

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

Journal of Bacteriology ◽

10.1128/jb.00215-15 ◽

2015 ◽

Vol 197 (14) ◽

pp. 2412-2421 ◽

Cited By ~ 18

Author(s):

Ryan Sturms ◽

Nicholas A. Streauslin ◽

Shouqiang Cheng ◽

Thomas A. Bobik

Keyword(s):

Protein Interactions ◽

Regulatory Protein ◽

Gene Clusters ◽

Content Type ◽

Bacterial Microcompartments ◽

Shell Protein ◽

Bacterial Microcompartment ◽

Genes Encoding ◽

Shell Proteins ◽

High Conservation

ABSTRACTBacterial microcompartments (MCPs) are a diverse family of protein-based organelles composed of metabolic enzymes encapsulated within a protein shell. The function of bacterial MCPs is to optimize metabolic pathways by confining toxic and/or volatile metabolic intermediates. About 20% of bacteria produce MCPs, and there are at least seven different types. Different MCPs vary in their encapsulated enzymes, but all have outer shells composed of highly conserved proteins containing bacterial microcompartment domains. Many organisms have genes encoding more than one type of MCP, but given the high homology among shell proteins, it is uncertain whether multiple MCPs can be functionally expressed in the same cell at the same time. In these studies, we examine the regulation of the 1,2-propanediol (1,2-PD) utilization (Pdu) and ethanolamine utilization (Eut) MCPs inSalmonella. Studies showed that 1,2-PD (shown to induce the Pdu MCP) represses transcription of the Eut MCP and that the PocR regulatory protein is required. The results indicate that repression of the Eut MCP by 1,2-PD is needed to prevent detrimental mixing of shell proteins from the Eut and Pdu MCPs. Coexpression of both MCPs impaired the function of the Pdu MCP and resulted in the formation of hybrid MCPs composed of Eut and Pdu MCP components. We also show that plasmid-based expression of individual shell proteins from the Eut MCP or the β-carboxysome impaired the function of Pdu MCP. Thus, the high conservation among bacterial microcompartment (BMC) domain shell proteins is problematic for coexpression of the Eut and Pdu MCPs and perhaps other MCPs as well.IMPORTANCEBacterial MCPs are encoded by nearly 20% of bacterial genomes, and almost 40% of those genomes contain multiple MCP gene clusters. In this study, we examine how the regulation of two different MCP systems (Eut and Pdu) is integrated inSalmonella. Our findings indicate that 1,2-PD (shown to induce the Pdu MCP) represses the Eut MCP to prevent detrimental mixing of Eut and Pdu shell proteins. These findings suggest that numerous organisms which produce more than one type of MCP likely need some mechanism to prevent aberrant shell protein interactions.

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A Transcriptomic Approach to the Metabolism of Tetrapyrrolic Photosensitizers in a Marine Annelid

Molecules ◽

10.3390/molecules26133924 ◽

2021 ◽

Vol 26 (13) ◽

pp. 3924

Author(s):

Maria Leonor Santos ◽

Mariaelena D’Ambrosio ◽

Ana P. Rodrigo ◽

A. Jorge Parola ◽

Pedro M. Costa

Keyword(s):

Metabolic Pathways ◽

Molecular Networks ◽

Bile Pigments ◽

Rna Seq ◽

The Past ◽

Wide Range ◽

Genes Encoding ◽

Organ Specific ◽

Bright Green ◽

Green Coloration

The past decade has seen growing interest in marine natural pigments for biotechnological applications. One of the most abundant classes of biological pigments is the tetrapyrroles, which are prized targets due their photodynamic properties; porphyrins are the best known examples of this group. Many animal porphyrinoids and other tetrapyrroles are produced through heme metabolic pathways, the best known of which are the bile pigments biliverdin and bilirubin. Eulalia is a marine Polychaeta characterized by its bright green coloration resulting from a remarkably wide range of greenish and yellowish tetrapyrroles, some of which have promising photodynamic properties. The present study combined metabolomics based on HPLC-DAD with RNA-seq transcriptomics to investigate the molecular pathways of porphyrinoid metabolism by comparing the worm’s proboscis and epidermis, which display distinct pigmentation patterns. The results showed that pigments are endogenous and seemingly heme-derived. The worm possesses homologs in both organs for genes encoding enzymes involved in heme metabolism such as ALAD, FECH, UROS, and PPOX. However, the findings also indicate that variants of the canonical enzymes of the heme biosynthesis pathway can be species- and organ-specific. These differences between molecular networks contribute to explain not only the differential pigmentation patterns between organs, but also the worm’s variety of novel endogenous tetrapyrrolic compounds.

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Mutagenesis of the C1 Oxidation Pathway in Methanosarcina barkeri: New Insights into the Mtr/Mer Bypass Pathway

Journal of Bacteriology ◽

10.1128/jb.01424-07 ◽

2008 ◽

Vol 190 (6) ◽

pp. 1928-1936 ◽

Cited By ~ 33

Author(s):

Paula V. Welander ◽

William W. Metcalf

Keyword(s):

Metabolic Pathways ◽

Methanosarcina Barkeri ◽

Growth Substrate ◽

Oxidation Of Methanol ◽

Cell Extracts ◽

Oxidation Reduction ◽

Absolute Requirement ◽

Genes Encoding ◽

Encoding Gene

ABSTRACT A series of Methanosarcina barkeri mutants lacking the genes encoding the enzymes involved in the C1 oxidation/reduction pathway were constructed. Mutants lacking the methyl-tetrahydromethanopterin (H4MPT):coenzyme M (CoM) methyltransferase-encoding operon (Δmtr), the methylene-H4MPT reductase-encoding gene (Δmer), the methylene-H4MPT dehydrogenase-encoding gene (Δmtd), and the formyl-methanofuran:H4MPT formyl-transferase-encoding gene (Δftr) all failed to grow using either methanol or H2/CO2 as a growth substrate, indicating that there is an absolute requirement for the C1 oxidation/reduction pathway for hydrogenotrophic and methylotrophic methanogenesis. The mutants also failed to grow on acetate, and we suggest that this was due to an inability to generate the reducing equivalents needed for biosynthetic reactions. Despite their lack of growth on methanol, the Δmtr and Δmer mutants were capable of producing methane from this substrate, whereas the Δmtd and Δftr mutants were not. Thus, there is an Mtr/Mer bypass pathway that allows oxidation of methanol to the level of methylene-H4MPT in M. barkeri. The data further suggested that formaldehyde may be an intermediate in this bypass; however, no methanol dehydrogenase activity was found in Δmtr cell extracts, nor was there an obligate role for the formaldehyde-activating enzyme (Fae), which has been shown to catalyze the condensation of formaldehyde and H4MPT in vitro. Both the Δmer and Δmtr mutants were able to grow on a combination of methanol plus acetate, but they did so by metabolic pathways that are clearly distinct from each other and from previously characterized methanogenic pathways.

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Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1207516109 ◽

2012 ◽

Vol 109 (37) ◽

pp. 14995-15000 ◽

Cited By ~ 83

Author(s):

C. Fan ◽

S. Cheng ◽

S. Sinha ◽

T. A. Bobik

Keyword(s):

Bacterial Microcompartments ◽

Enzyme Encapsulation ◽

Shell Proteins

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Adaptation of Corynebacterium glutamicum to Ammonium Limitation: a Global Analysis Using Transcriptome and Proteome Techniques

Applied and Environmental Microbiology ◽

10.1128/aem.71.5.2391-2402.2005 ◽

2005 ◽

Vol 71 (5) ◽

pp. 2391-2402 ◽

Cited By ~ 50

Author(s):

Maike Silberbach ◽

Mathias Schäfer ◽

Andrea T. Hüser ◽

Jörn Kalinowski ◽

Alfred Pühler ◽

...

Keyword(s):

Corynebacterium Glutamicum ◽

Metabolic Pathways ◽

Ribosomal Proteins ◽

Nitrogen Assimilation ◽

Global Analysis ◽

Cellular Transport ◽

Acid Biosynthesis ◽

Limited Growth ◽

Rate Dependent ◽

Genes Encoding

ABSTRACT Theresponse of Corynebacterium glutamicum to ammonium limitation was studied by transcriptional and proteome profiling of cells grown in a chemostat. Our results show that ammonium-limited growth of C. glutamicum results in a rearrangement of the cellular transport capacity, changes in metabolic pathways for nitrogen assimilation, amino acid biosynthesis, and carbon metabolism, as well as a decreased cell division. Since transcription at different growth rates was studied, it was possible to distinguish specific responses to ammonium limitation and more general, growth rate-dependent alterations in gene expression. The latter include a number of genes encoding ribosomal proteins and genes for FoF1-ATP synthase subunits.

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