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Title: Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications

Journal Article · · Frontiers in Microbiology
 [1];  [1];  [2];  [2];  [2];  [3];  [1]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Computational Sciences and Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences (CNMS)
  3. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

As synthetic biology advances the intricacy of engineered biological systems, the importance of spatial organization within the cellular environment must not be marginalized. Increasingly, biological engineers are investigating means to control spatial organization within the cell, mimicking strategies used by natural pathways to increase flux and reduce cross-talk. A modular platform for constructing a diverse set of defined, programmable architectures would greatly assist in improving yields from introduced metabolic pathways and increasing insulation of other heterologous systems. Here, we review recent research on the shell proteins of bacterial microcompartments and discuss their potential application as “building blocks” for a range of customized intracellular scaffolds. As a result, we summarize the state of knowledge on the self-assembly of BMC shell proteins and discuss future avenues of research that will be important to realize the potential of BMC shell proteins as predictively assembling and programmable biological materials for bioengineering.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC05-00OR22725; FG02-91ER20021
OSTI ID:
1399948
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 8; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (147)

A rapid flow cytometry assay for the relative quantification of protein encapsulation into bacterial microcompartments journal January 2014
Engineering bacterial microcompartments with heterologous enzyme cargos journal September 2016
Insights from multiple structures of the shell proteins from the β-carboxysome journal January 2008
Two-dimensional crystals of carboxysome shell proteins recapitulate the hexagonal packing of three-dimensional crystals journal December 2009
Encapsulation of multiple cargo proteins within recombinant Eut nanocompartments journal July 2016
Comparative analysis of carboxysome shell proteins journal January 2011
Interactions and structural variability of β-carboxysomal shell protein CcmL journal February 2014
Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway journal November 2013
Engineering the spatial organization of metabolic enzymes: mimicking nature's synergy journal October 2008
Rationally engineering natural protein assemblies in nanobiotechnology journal August 2011
Engineering enzymatic cascades on nanoscale scaffolds journal August 2013
Synthetic scaffolds for pathway enhancement journal December 2015
Heterologous expression of the Halothiobacillus neapolitanus carboxysomal gene cluster in Corynebacterium glutamicum journal September 2017
Assembly of Robust Bacterial Microcompartment Shells Using Building Blocks from an Organelle of Unknown Function journal May 2014
Alanine Scanning Mutagenesis Identifies an Asparagine–Arginine–Lysine Triad Essential to Assembly of the Shell of the Pdu Microcompartment journal June 2014
Encapsulation as a Strategy for the Design of Biological Compartmentalization journal February 2016
Synthesis of Empty Bacterial Microcompartments, Directed Organelle Protein Incorporation, and Evidence of Filament-Associated Organelle Movement journal April 2010
A Dodecameric CcmK2 Structure Suggests β-Carboxysomal Shell Facets Have a Double-Layered Organization journal August 2012
Bacterial microcompartments and the modular construction of microbial metabolism journal January 2015
Spatial organization of enzymes for metabolic engineering journal May 2012
Employing bacterial microcompartment technology to engineer a shell-free enzyme-aggregate for enhanced 1,2-propanediol production in Escherichia coli journal July 2016
Protein Assembly: Versatile Approaches to Construct Highly Ordered Nanostructures journal September 2016
Protein Calligraphy: A New Concept Begins To Take Shape journal June 2016
Theoretical Study of the Initial Stages of Self-Assembly of a Carboxysome’s Facet journal March 2016
Evidence for Improved Encapsulated Pathway Behavior in a Bacterial Microcompartment through Shell Protein Engineering journal June 2017
Interenzyme Substrate Diffusion for an Enzyme Cascade Organized on Spatially Addressable DNA Nanostructures journal March 2012
Channeling by Proximity: The Catalytic Advantages of Active Site Colocalization Using Brownian Dynamics journal April 2010
Solution Structure of a Bacterial Microcompartment Targeting Peptide and Its Application in the Construction of an Ethanol Bioreactor journal November 2013
Engineering Bacterial Microcompartment Shells: Chimeric Shell Proteins and Chimeric Carboxysome Shells journal July 2014
Enzyme clustering accelerates processing of intermediates through metabolic channeling journal September 2014
Substrate channelling as an approach to cascade reactions journal March 2016
Natural strategies for the spatial optimization of metabolism in synthetic biology journal May 2012
Genetic encoding of DNA nanostructures and their self-assembly in living bacteria journal April 2016
Undesired usage and the robust self-assembly of heterogeneous structures journal February 2015
Enzyme cascades activated on topologically programmed DNA scaffolds journal March 2009
Challenges and opportunities for structural DNA nanotechnology journal November 2011
Placing molecules with Bohr radius resolution using DNA origami journal October 2015
Using synthetic RNAs as scaffolds and regulators journal January 2015
Engineering formation of multiple recombinant Eut protein nanocompartments in E. coli journal April 2016
Structure of a novel 13 nm dodecahedral nanocage assembled from a redesigned bacterial microcompartment shell protein journal January 2016
Modularity of a carbon-fixing protein organelle journal December 2011
Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments journal August 2012
An iterative method for extracting energy-like quantities from protein structures. journal October 1996
Structural Insight into the Mechanisms of Transport across the Salmonella enterica Pdu Microcompartment Shell journal September 2010
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment journal April 2013
Structural Insights into Higher Order Assembly and Function of the Bacterial Microcompartment Protein PduA journal May 2014
Localization of Proteins to the 1,2-Propanediol Utilization Microcompartment by Non-native Signal Sequences Is Mediated by a Common Hydrophobic Motif journal August 2015
DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency journal October 2011
Light Modulates the Biosynthesis and Organization of Cyanobacterial Carbon Fixation Machinery through Photosynthetic Electron Flow journal March 2016
Streamlined Construction of the Cyanobacterial CO 2 -Fixing Organelle via Protein Domain Fusions for Use in Plant Synthetic Biology journal August 2015
The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene: Function of the PduJ microcompartment shell protein journal June 2016
β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts journal June 2014
Protein Structures Forming the Shell of Primitive Bacterial Organelles journal August 2005
Atomic-Level Models of the Bacterial Carboxysome Shell journal February 2008
Scaffold Proteins: Hubs for Controlling the Flow of Cellular Information journal May 2011
Signaling Through Scaffold, Anchoring, and Adaptor Proteins journal December 1997
Principles of assembly reveal a periodic table of protein complexes journal December 2015
Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell journal June 2017
Crystallographic Insights into the Pore Structures and Mechanisms of the EutL and EutM Shell Proteins of the Ethanolamine-Utilizing Microcompartment of Escherichia coli journal September 2010
PduA Is a Shell Protein of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2 journal March 2002
Rewiring Cells: Synthetic Biology as a Tool to Interrogate the Organizational Principles of Living Systems journal April 2010
Bacterial Microcompartment Organelles: Protein Shell Structure and Evolution journal April 2010
Bacterial Microcompartments journal October 2010
Re-directing bacterial microcompartment systems to enhance recombinant expression of lysis protein E from bacteriophage ϕX174 in Escherichia coli journal April 2017
A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method journal October 2014
Engineered Protein Nano-Compartments for Targeted Enzyme Localization journal March 2012
Structural Insight into the Clostridium difficile Ethanolamine Utilisation Microcompartment journal October 2012
A rapid flow cytometry assay for the relative quantification of protein encapsulation into bacterial microcompartments journal January 2014
Bacterial microcompartment-directed polyphosphate kinase promotes stable polyphosphate accumulation in E. coli journal February 2017
Engineering bacterial microcompartments with heterologous enzyme cargos journal September 2016
Insights from multiple structures of the shell proteins from the β-carboxysome journal January 2008
Two-dimensional crystals of carboxysome shell proteins recapitulate the hexagonal packing of three-dimensional crystals journal December 2009
Encapsulation of multiple cargo proteins within recombinant Eut nanocompartments journal July 2016
Comparative analysis of carboxysome shell proteins journal January 2011
Interactions and structural variability of β-carboxysomal shell protein CcmL journal February 2014
Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway journal November 2013
Engineering the spatial organization of metabolic enzymes: mimicking nature's synergy journal October 2008
Rationally engineering natural protein assemblies in nanobiotechnology journal August 2011
Engineering enzymatic cascades on nanoscale scaffolds journal August 2013
Synthetic scaffolds for pathway enhancement journal December 2015
Heterologous expression of the Halothiobacillus neapolitanus carboxysomal gene cluster in Corynebacterium glutamicum journal September 2017
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport journal September 2009
Assembly of Robust Bacterial Microcompartment Shells Using Building Blocks from an Organelle of Unknown Function journal May 2014
Alanine Scanning Mutagenesis Identifies an Asparagine–Arginine–Lysine Triad Essential to Assembly of the Shell of the Pdu Microcompartment journal June 2014
Encapsulation as a Strategy for the Design of Biological Compartmentalization journal February 2016
Synthesis of Empty Bacterial Microcompartments, Directed Organelle Protein Incorporation, and Evidence of Filament-Associated Organelle Movement journal April 2010
A Dodecameric CcmK2 Structure Suggests β-Carboxysomal Shell Facets Have a Double-Layered Organization journal August 2012
Bacterial microcompartments and the modular construction of microbial metabolism journal January 2015
Spatial organization of enzymes for metabolic engineering journal May 2012
Employing bacterial microcompartment technology to engineer a shell-free enzyme-aggregate for enhanced 1,2-propanediol production in Escherichia coli journal July 2016
Protein Assembly: Versatile Approaches to Construct Highly Ordered Nanostructures journal September 2016
Visualization of Bacterial Microcompartment Facet Assembly Using High-Speed Atomic Force Microscopy journal December 2015
Protein Calligraphy: A New Concept Begins To Take Shape journal June 2016
Theoretical Study of the Initial Stages of Self-Assembly of a Carboxysome’s Facet journal March 2016
Evidence for Improved Encapsulated Pathway Behavior in a Bacterial Microcompartment through Shell Protein Engineering journal June 2017
Principles of Protein−Protein Interactions: What are the Preferred Ways For Proteins To Interact? journal April 2008
Interenzyme Substrate Diffusion for an Enzyme Cascade Organized on Spatially Addressable DNA Nanostructures journal March 2012
Channeling by Proximity: The Catalytic Advantages of Active Site Colocalization Using Brownian Dynamics journal April 2010
Solution Structure of a Bacterial Microcompartment Targeting Peptide and Its Application in the Construction of an Ethanol Bioreactor journal November 2013
Engineering Bacterial Microcompartment Shells: Chimeric Shell Proteins and Chimeric Carboxysome Shells journal July 2014
Synthetic protein scaffolds provide modular control over metabolic flux journal August 2009
Enzyme clustering accelerates processing of intermediates through metabolic channeling journal September 2014
Substrate channelling as an approach to cascade reactions journal March 2016
Natural strategies for the spatial optimization of metabolism in synthetic biology journal May 2012
Genetic encoding of DNA nanostructures and their self-assembly in living bacteria journal April 2016
Undesired usage and the robust self-assembly of heterogeneous structures journal February 2015
Enzyme cascades activated on topologically programmed DNA scaffolds journal March 2009
Challenges and opportunities for structural DNA nanotechnology journal November 2011
Placing molecules with Bohr radius resolution using DNA origami journal October 2015
Using synthetic RNAs as scaffolds and regulators journal January 2015
Engineering formation of multiple recombinant Eut protein nanocompartments in E. coli journal April 2016
Structure of a novel 13 nm dodecahedral nanocage assembled from a redesigned bacterial microcompartment shell protein journal January 2016
Structure of a trimeric bacterial microcompartment shell protein, EtuB, associated with ethanol utilization in Clostridium kluyveri journal September 2009
Modularity of a carbon-fixing protein organelle journal December 2011
Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments journal August 2012
An iterative method for extracting energy-like quantities from protein structures. journal October 1996
Structural Insight into the Mechanisms of Transport across the Salmonella enterica Pdu Microcompartment Shell journal September 2010
Elucidating Essential Role of Conserved Carboxysomal Protein CcmN Reveals Common Feature of Bacterial Microcompartment Assembly journal March 2012
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment journal April 2013
Structural Insights into Higher Order Assembly and Function of the Bacterial Microcompartment Protein PduA journal May 2014
Localization of Proteins to the 1,2-Propanediol Utilization Microcompartment by Non-native Signal Sequences Is Mediated by a Common Hydrophobic Motif journal August 2015
Biochemical and Structural Insights into Bacterial Organelle Form and Biogenesis journal March 2008
Bacterial microcompartment assembly: The key role of encapsulation peptides journal May 2015
DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency journal October 2011
Light Modulates the Biosynthesis and Organization of Cyanobacterial Carbon Fixation Machinery through Photosynthetic Electron Flow journal March 2016
Streamlined Construction of the Cyanobacterial CO 2 -Fixing Organelle via Protein Domain Fusions for Use in Plant Synthetic Biology journal August 2015
The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene: Function of the PduJ microcompartment shell protein journal June 2016
β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts journal June 2014
Protein Structures Forming the Shell of Primitive Bacterial Organelles journal August 2005
Atomic-Level Models of the Bacterial Carboxysome Shell journal February 2008
Spatially Ordered Dynamics of the Bacterial Carbon Fixation Machinery journal March 2010
Scaffold Proteins: Hubs for Controlling the Flow of Cellular Information journal May 2011
Signaling Through Scaffold, Anchoring, and Adaptor Proteins journal December 1997
Principles of assembly reveal a periodic table of protein complexes journal December 2015
Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell journal June 2017
Crystallographic Insights into the Pore Structures and Mechanisms of the EutL and EutM Shell Proteins of the Ethanolamine-Utilizing Microcompartment of Escherichia coli journal September 2010
PduA Is a Shell Protein of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2 journal March 2002
Bacterial Microcompartments journal January 2007
Rewiring Cells: Synthetic Biology as a Tool to Interrogate the Organizational Principles of Living Systems journal April 2010
Bacterial Microcompartment Organelles: Protein Shell Structure and Evolution journal April 2010
Bacterial Microcompartments journal October 2010
Re-directing bacterial microcompartment systems to enhance recombinant expression of lysis protein E from bacteriophage ϕX174 in Escherichia coli journal April 2017
A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method journal October 2014
Engineered Protein Nano-Compartments for Targeted Enzyme Localization journal March 2012
Structural Insight into the Clostridium difficile Ethanolamine Utilisation Microcompartment journal October 2012
Synthetic Protein Scaffolds Based on Peptide Motifs and Cognate Adaptor Domains for Improving Metabolic Productivity journal November 2015
Many-molecule encapsulation by an icosahedral shell journal May 2016

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Engineering substrate channeling in biosystems for improved efficiency: Approaches to engineering substrate channeling journal June 2018
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Deciphering molecular details in the assembly of alpha-type carboxysome journal October 2018
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Occurrence and stability of hetero-hexamer associations formed by β-carboxysome CcmK shell components journal October 2019
Protein Gradients on the Nucleoid Position the Carbon-Fixing Organelles of Cyanobacteria journal January 2018
Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme journal January 2020
Occurrence and stability of hetero-hexamer associations formed by β-carboxysome CcmK shell components text January 2019
Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria journal December 2018