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Title: Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications

Abstract

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.

Authors:
 [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). Molecular Biophysics and Integrated Bioimaging Division
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1399948
Alternate Identifier(s):
OSTI ID: 1687363
Grant/Contract Number:  
AC05-00OR22725; FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; scaffold; synthetic biology; bacterial microcompartment; shell proteins; BMC; spatial organization; metabolic engineering; self-assembly

Citation Formats

Young, Eric J., Burton, Rodney, Mahalik, Jyoti P., Sumpter, Bobby G., Fuentes-Cabrera, Miguel, Kerfeld, Cheryl A., and Ducat, Daniel C. Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01441.
Young, Eric J., Burton, Rodney, Mahalik, Jyoti P., Sumpter, Bobby G., Fuentes-Cabrera, Miguel, Kerfeld, Cheryl A., & Ducat, Daniel C. Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications. United States. https://doi.org/10.3389/fmicb.2017.01441
Young, Eric J., Burton, Rodney, Mahalik, Jyoti P., Sumpter, Bobby G., Fuentes-Cabrera, Miguel, Kerfeld, Cheryl A., and Ducat, Daniel C. Mon . "Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications". United States. https://doi.org/10.3389/fmicb.2017.01441. https://www.osti.gov/servlets/purl/1399948.
@article{osti_1399948,
title = {Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications},
author = {Young, Eric J. and Burton, Rodney and Mahalik, Jyoti P. and Sumpter, Bobby G. and Fuentes-Cabrera, Miguel and Kerfeld, Cheryl A. and Ducat, Daniel C.},
abstractNote = {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.},
doi = {10.3389/fmicb.2017.01441},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Mon Jul 31 00:00:00 EDT 2017},
month = {Mon Jul 31 00:00:00 EDT 2017}
}

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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

  • Lassila, Jonathan K.; Bernstein, Susan L.; Kinney, James N.
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Alanine Scanning Mutagenesis Identifies an Asparagine–Arginine–Lysine Triad Essential to Assembly of the Shell of the Pdu Microcompartment
journal, June 2014

  • Sinha, Sharmistha; Cheng, Shouqiang; Sung, Yea Won
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Encapsulation as a Strategy for the Design of Biological Compartmentalization
journal, February 2016


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


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

  • Slininger Lee, Marilyn F.; Jakobson, Christopher M.; Tullman-Ercek, Danielle
  • ACS Synthetic Biology, Vol. 6, Issue 10
  • DOI: 10.1021/acssynbio.7b00042

Interenzyme Substrate Diffusion for an Enzyme Cascade Organized on Spatially Addressable DNA Nanostructures
journal, March 2012

  • Fu, Jinglin; Liu, Minghui; Liu, Yan
  • Journal of the American Chemical Society, Vol. 134, Issue 12
  • DOI: 10.1021/ja300897h

Channeling by Proximity: The Catalytic Advantages of Active Site Colocalization Using Brownian Dynamics
journal, April 2010

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  • The Journal of Physical Chemistry Letters, Vol. 1, Issue 9
  • DOI: 10.1021/jz1002007

Solution Structure of a Bacterial Microcompartment Targeting Peptide and Its Application in the Construction of an Ethanol Bioreactor
journal, November 2013

  • Lawrence, Andrew D.; Frank, Stefanie; Newnham, Sarah
  • ACS Synthetic Biology, Vol. 3, Issue 7
  • DOI: 10.1021/sb4001118

Engineering Bacterial Microcompartment Shells: Chimeric Shell Proteins and Chimeric Carboxysome Shells
journal, July 2014

  • Cai, Fei; Sutter, Markus; Bernstein, Susan L.
  • ACS Synthetic Biology, Vol. 4, Issue 4
  • DOI: 10.1021/sb500226j

Enzyme clustering accelerates processing of intermediates through metabolic channeling
journal, September 2014

  • Castellana, Michele; Wilson, Maxwell Z.; Xu, Yifan
  • Nature Biotechnology, Vol. 32, Issue 10
  • DOI: 10.1038/nbt.3018

Substrate channelling as an approach to cascade reactions
journal, March 2016

  • Wheeldon, Ian; Minteer, Shelley D.; Banta, Scott
  • Nature Chemistry, Vol. 8, Issue 4
  • DOI: 10.1038/nchem.2459

Natural strategies for the spatial optimization of metabolism in synthetic biology
journal, May 2012

  • Agapakis, Christina M.; Boyle, Patrick M.; Silver, Pamela A.
  • Nature Chemical Biology, Vol. 8, Issue 6
  • DOI: 10.1038/nchembio.975

Genetic encoding of DNA nanostructures and their self-assembly in living bacteria
journal, April 2016

  • Elbaz, Johann; Yin, Peng; Voigt, Christopher A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11179

Undesired usage and the robust self-assembly of heterogeneous structures
journal, February 2015

  • Murugan, Arvind; Zou, James; Brenner, Michael P.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7203

Enzyme cascades activated on topologically programmed DNA scaffolds
journal, March 2009

  • Wilner, Ofer I.; Weizmann, Yossi; Gill, Ron
  • Nature Nanotechnology, Vol. 4, Issue 4
  • DOI: 10.1038/nnano.2009.50

Challenges and opportunities for structural DNA nanotechnology
journal, November 2011

  • Pinheiro, Andre V.; Han, Dongran; Shih, William M.
  • Nature Nanotechnology, Vol. 6, Issue 12
  • DOI: 10.1038/nnano.2011.187

Placing molecules with Bohr radius resolution using DNA origami
journal, October 2015


Using synthetic RNAs as scaffolds and regulators
journal, January 2015

  • Myhrvold, Cameron; Silver, Pamela A.
  • Nature Structural & Molecular Biology, Vol. 22, Issue 1
  • DOI: 10.1038/nsmb.2944

Engineering formation of multiple recombinant Eut protein nanocompartments in E. coli
journal, April 2016

  • Held, Mark; Kolb, Alexander; Perdue, Sarah
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep24359

Modularity of a carbon-fixing protein organelle
journal, December 2011

  • Bonacci, W.; Teng, P. K.; Afonso, B.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 2
  • DOI: 10.1073/pnas.1108557109

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