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Title: Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell

Journal Article · · Science

Many bacteria contain primitive organelles composed entirely of protein. These bacterial microcompartments share a common architecture of an enzymatic core encapsulated in a selectively permeable protein shell; prominent examples include the carboxysome for CO2 fixation and catabolic microcompartments found in many pathogenic microbes. The shell sequesters enzymatic reactions from the cytosol, analogous to the lipid-based membrane of eukaryotic organelles. Despite available structural information for single building blocks, the principles of shell assembly have remained elusive. Here, we present the crystal structure of an intact shell from Haliangium ochraceum, revealing the basic principles of bacterial microcompartment shell construction. Because of the conservation among shell proteins of all bacterial microcompartments, these principles apply to functionally diverse organelles and can inform the design and engineering of shells with new functionalities.

Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Univ. of California, Berkeley, CA (United States); Stanford Univ., CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Swiss National Science Foundation (SNSF)
Grant/Contract Number:
FG02-91ER20021; 1R01AI114975-01; AC02-05CH11231; AC02-76SF00515
OSTI ID:
1434339
Alternate ID(s):
OSTI ID: 1596315
Journal Information:
Science, Journal Name: Science Vol. 356 Journal Issue: 6344; ISSN 0036-8075
Publisher:
AAASCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 115 works
Citation information provided by
Web of Science

References (30)

Linking Crystallographic Model and Data Quality journal May 2012
Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single-particle Electron Cryomicroscopy journal October 2003
Functional Organelles in Prokaryotes: Polyhedral Inclusions (Carboxysomes) of Thiobacillus neapolitanus journal November 1973
Overview of the CCP 4 suite and current developments journal March 2011
Bacterial microcompartment assembly: The key role of encapsulation peptides journal May 2015
Clustal W and Clustal X version 2.0 journal September 2007
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 journal March 2010
DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy journal May 2009
Prevention of overfitting in cryo-EM structure determination journal July 2012
RELION: Implementation of a Bayesian approach to cryo-EM structure determination journal December 2012
Appion: An integrated, database-driven pipeline to facilitate EM image processing journal April 2009
Automated molecular microscopy: The new Leginon system journal July 2005
Structure and Mechanisms of a Protein-Based Organelle in Escherichia coli journal December 2009
Towards automated crystallographic structure refinement with phenix.refine journal March 2012
The E. coli BtuCD Structure: A Framework for ABC Transporter Architecture and Mechanism journal May 2002
Structure and Function of a Bacterial Microcompartment Shell Protein Engineered to Bind a [4Fe-4S] Cluster journal January 2016
CTFFIND4: Fast and accurate defocus estimation from electron micrographs journal November 2015
A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method journal October 2014
The infectious particle of insect-borne totivirus-like Omono River virus has raised ridges and lacks fibre complexes journal September 2016
Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome journal May 2007
Assembly of Robust Bacterial Microcompartment Shells Using Building Blocks from an Organelle of Unknown Function journal May 2014
Atomic-Level Models of the Bacterial Carboxysome Shell journal February 2008
Visualization of Bacterial Microcompartment Facet Assembly Using High-Speed Atomic Force Microscopy journal December 2015
XDS journal January 2010
UCSF Chimera?A visualization system for exploratory research and analysis journal January 2004
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport journal September 2009
A Complete Structural Inventory of the Mycobacterial Microcompartment Shell Proteins Constrains Models of Global Architecture and Transport journal December 2016
Unique Thylakoid Membrane Architecture of a Unicellular N 2 -Fixing Cyanobacterium Revealed by Electron Tomography journal December 2010
Protein Structures Forming the Shell of Primitive Bacterial Organelles journal August 2005
phyloXML: XML for evolutionary biology and comparative genomics journal October 2009

Cited By (34)

Multicomponent Self-Assembly of Metallo-Supramolecular Macrocycles and Cages through Dynamic Heteroleptic Terpyridine Complexation journal June 2018
A Generic Self-Assembly Process in Microcompartments and Synthetic Protein Nanotubes journal March 2018
Building a toolbox of protein scaffolds for future immobilization of biocatalysts journal July 2018
Engineered synthetic scaffolds for organizing proteins within the bacterial cytoplasm journal December 2017
Bacterial microcompartments journal March 2018
Prokaryotic nanocompartments form synthetic organelles in a eukaryote journal April 2018
Programmed loading and rapid purification of engineered bacterial microcompartment shells journal July 2018
De novo targeting to the cytoplasmic and luminal side of bacterial microcompartments journal August 2018
Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts journal September 2018
Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles journal January 2020
Comparing proteins and nucleic acids for next-generation biomolecular engineering journal July 2018
The multicatalytic compartment of propionyl-CoA synthase sequesters a toxic metabolite journal October 2018
SnoopLigase peptide-peptide conjugation enables modular vaccine assembly journal March 2019
Structural nanotechnology: three-dimensional cryo-EM and its use in the development of nanoplatforms for in vitro catalysis journal January 2019
Functional protein shells fabricated from the self-assembling protein sheets of prokaryotic organelles journal January 2020
Bio-engineering of bacterial microcompartments: a mini review journal June 2019
Structural and kinetic characterization of ( S )-1-amino-2-propanol kinase from the aminoacetone utilization microcompartment of Mycobacterium smegmatis journal October 2018
The small RbcS-like domains of the β-carboxysome structural protein CcmM bind RubisCO at a site distinct from that binding the RbcS subunit journal December 2018
Fast normal mode computations of capsid dynamics inspired by resonance journal April 2018
Symmetry considerations elucidate the roles of global shape and local interactions in the equilibrium fluctuations and cooperativity of protein assemblies journal April 2019
Carboxysomes: metabolic modules for CO2 fixation journal August 2017
Engineering the PduT shell protein to modify the permeability of the 1,2-propanediol microcompartment of Salmonella journal December 2019
Harnessing the power of microbial nanowires journal May 2018
A Bacterial Microcompartment Is Used for Choline Fermentation by Escherichia coli 536 journal March 2018
Glycyl Radical Enzyme-Associated Microcompartments: Redox-Replete Bacterial Organelles journal January 2019
RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon journal January 2018
Self-Assembly Stability and Variability of Bacterial Microcompartment Shell Proteins in Response to the Environmental Change journal February 2019
Cellular origin of the viral capsid-like bacterial microcompartments journal November 2017
The role of the encapsulated cargo in microcompartment assembly journal July 2018
All-atom normal mode dynamics of HIV-1 capsid journal September 2018
Occurrence and stability of hetero-hexamer associations formed by β-carboxysome CcmK shell components journal October 2019
Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme journal January 2020
Comparative Genomic Analysis Reveals Novel Microcompartment-Associated Metabolic Pathways in the Human Gut Microbiome journal July 2019
Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications journal July 2017

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