Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell
Abstract
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.
- Authors:
- Publication Date:
- Research Org.:
- 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 Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Swiss National Science Foundation (SNSF)
- OSTI Identifier:
- 1434339
- Alternate Identifier(s):
- OSTI ID: 1596315
- Grant/Contract Number:
- FG02-91ER20021; 1R01AI114975-01; AC02-05CH11231; AC02-76SF00515
- Resource Type:
- Published Article
- Journal Name:
- Science
- Additional Journal Information:
- Journal Name: Science Journal Volume: 356 Journal Issue: 6344; Journal ID: ISSN 0036-8075
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Sutter, Markus, Greber, Basil, Aussignargues, Clement, and Kerfeld, Cheryl A. Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell. United States: N. p., 2017.
Web. doi:10.1126/science.aan3289.
Sutter, Markus, Greber, Basil, Aussignargues, Clement, & Kerfeld, Cheryl A. Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell. United States. https://doi.org/10.1126/science.aan3289
Sutter, Markus, Greber, Basil, Aussignargues, Clement, and Kerfeld, Cheryl A. Thu .
"Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell". United States. https://doi.org/10.1126/science.aan3289.
@article{osti_1434339,
title = {Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell},
author = {Sutter, Markus and Greber, Basil and Aussignargues, Clement and Kerfeld, Cheryl A.},
abstractNote = {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.},
doi = {10.1126/science.aan3289},
journal = {Science},
number = 6344,
volume = 356,
place = {United States},
year = {Thu Jun 22 00:00:00 EDT 2017},
month = {Thu Jun 22 00:00:00 EDT 2017}
}
https://doi.org/10.1126/science.aan3289
Web of Science
Works referenced in this record:
Linking Crystallographic Model and Data Quality
journal, May 2012
- Karplus, P. A.; Diederichs, K.
- Science, Vol. 336, Issue 6084
Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single-particle Electron Cryomicroscopy
journal, October 2003
- Rosenthal, Peter B.; Henderson, Richard
- Journal of Molecular Biology, Vol. 333, Issue 4
Functional Organelles in Prokaryotes: Polyhedral Inclusions (Carboxysomes) of Thiobacillus neapolitanus
journal, November 1973
- Shively, J. M.; Ball, F.; Brown, D. H.
- Science, Vol. 182, Issue 4112
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Bacterial microcompartment assembly: The key role of encapsulation peptides
journal, May 2015
- Aussignargues, Clément; Paasch, Bradley C.; Gonzalez-Esquer, Raul
- Communicative & Integrative Biology, Vol. 8, Issue 3
Clustal W and Clustal X version 2.0
journal, September 2007
- Larkin, M. A.; Blackshields, G.; Brown, N. P.
- Bioinformatics, Vol. 23, Issue 21, p. 2947-2948
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Systematic Biology, Vol. 59, Issue 3
DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy
journal, May 2009
- Voss, N. R.; Yoshioka, C. K.; Radermacher, M.
- Journal of Structural Biology, Vol. 166, Issue 2
Prevention of overfitting in cryo-EM structure determination
journal, July 2012
- Scheres, Sjors H. W.; Chen, Shaoxia
- Nature Methods, Vol. 9, Issue 9
RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012
- Scheres, Sjors H. W.
- Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530
Appion: An integrated, database-driven pipeline to facilitate EM image processing
journal, April 2009
- Lander, Gabriel C.; Stagg, Scott M.; Voss, Neil R.
- Journal of Structural Biology, Vol. 166, Issue 1
Automated molecular microscopy: The new Leginon system
journal, July 2005
- Suloway, Christian; Pulokas, James; Fellmann, Denis
- Journal of Structural Biology, Vol. 151, Issue 1
Structure and Mechanisms of a Protein-Based Organelle in Escherichia coli
journal, December 2009
- Tanaka, S.; Sawaya, M. R.; Yeates, T. O.
- Science, Vol. 327, Issue 5961
Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012
- Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
The E. coli BtuCD Structure: A Framework for ABC Transporter Architecture and Mechanism
journal, May 2002
- Locher, K. P.
- Science, Vol. 296, Issue 5570
Structure and Function of a Bacterial Microcompartment Shell Protein Engineered to Bind a [4Fe-4S] Cluster
journal, January 2016
- Aussignargues, Clément; Pandelia, Maria-Eirini; Sutter, Markus
- Journal of the American Chemical Society, Vol. 138, Issue 16
CTFFIND4: Fast and accurate defocus estimation from electron micrographs
journal, November 2015
- Rohou, Alexis; Grigorieff, Nikolaus
- Journal of Structural Biology, Vol. 192, Issue 2
A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method
journal, October 2014
- Axen, Seth D.; Erbilgin, Onur; Kerfeld, Cheryl A.
- PLoS Computational Biology, Vol. 10, Issue 10
The infectious particle of insect-borne totivirus-like Omono River virus has raised ridges and lacks fibre complexes
journal, September 2016
- Okamoto, Kenta; Miyazaki, Naoyuki; Larsson, Daniel S. D.
- Scientific Reports, Vol. 6, Issue 1
Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome
journal, May 2007
- Tsai, Yingssu; Sawaya, Michael R.; Cannon, Gordon C.
- PLoS Biology, Vol. 5, Issue 6
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.
- Journal of Molecular Biology, Vol. 426, Issue 11
Atomic-Level Models of the Bacterial Carboxysome Shell
journal, February 2008
- Tanaka, S.; Kerfeld, C. A.; Sawaya, M. R.
- Science, Vol. 319, Issue 5866
Visualization of Bacterial Microcompartment Facet Assembly Using High-Speed Atomic Force Microscopy
journal, December 2015
- Sutter, Markus; Faulkner, Matthew; Aussignargues, Clément
- Nano Letters, Vol. 16, Issue 3
XDS
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport
journal, September 2009
- Klein, Michael G.; Zwart, Peter; Bagby, Sarah C.
- Journal of Molecular Biology, Vol. 392, Issue 2
A Complete Structural Inventory of the Mycobacterial Microcompartment Shell Proteins Constrains Models of Global Architecture and Transport
journal, December 2016
- Mallette, Evan; Kimber, Matthew S.
- Journal of Biological Chemistry, Vol. 292, Issue 4
Unique Thylakoid Membrane Architecture of a Unicellular N 2 -Fixing Cyanobacterium Revealed by Electron Tomography
journal, December 2010
- Liberton, Michelle; Austin, Jotham R.; Berg, R. Howard
- Plant Physiology, Vol. 155, Issue 4
Protein Structures Forming the Shell of Primitive Bacterial Organelles
journal, August 2005
- Kerfeld, C. A.
- Science, Vol. 309, Issue 5736
phyloXML: XML for evolutionary biology and comparative genomics
journal, October 2009
- Han, Mira V.; Zmasek, Christian M.
- BMC Bioinformatics, Vol. 10, Issue 1
Works referencing / citing this record:
Multicomponent Self-Assembly of Metallo-Supramolecular Macrocycles and Cages through Dynamic Heteroleptic Terpyridine Complexation
journal, June 2018
- Wang, Shih-Yu; Huang, Jyun-Yang; Liang, Yen-Peng
- Chemistry - A European Journal, Vol. 24, Issue 37
A Generic Self-Assembly Process in Microcompartments and Synthetic Protein Nanotubes
journal, March 2018
- Uddin, Ismail; Frank, Stefanie; Warren, Martin J.
- Small, Vol. 14, Issue 19
Building a toolbox of protein scaffolds for future immobilization of biocatalysts
journal, July 2018
- Schmidt-Dannert, Sarah; Zhang, Guoqiang; Johnston, Timothy
- Applied Microbiology and Biotechnology, Vol. 102, Issue 19
Engineered synthetic scaffolds for organizing proteins within the bacterial cytoplasm
journal, December 2017
- Lee, Matthew J.; Mantell, Judith; Hodgson, Lorna
- Nature Chemical Biology, Vol. 14, Issue 2
Bacterial microcompartments
journal, March 2018
- Kerfeld, Cheryl A.; Aussignargues, Clement; Zarzycki, Jan
- Nature Reviews Microbiology, Vol. 16, Issue 5
Prokaryotic nanocompartments form synthetic organelles in a eukaryote
journal, April 2018
- Lau, Yu Heng; Giessen, Tobias W.; Altenburg, Wiggert J.
- Nature Communications, Vol. 9, Issue 1
Programmed loading and rapid purification of engineered bacterial microcompartment shells
journal, July 2018
- Hagen, Andrew; Sutter, Markus; Sloan, Nancy
- Nature Communications, Vol. 9, Issue 1
De novo targeting to the cytoplasmic and luminal side of bacterial microcompartments
journal, August 2018
- Lee, Matthew J.; Mantell, Judith; Brown, Ian R.
- Nature Communications, Vol. 9, Issue 1
Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts
journal, September 2018
- Long, Benedict M.; Hee, Wei Yih; Sharwood, Robert E.
- Nature Communications, Vol. 9, Issue 1
Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles
journal, January 2020
- Kalnins, Gints; Cesle, Eva-Emilija; Jansons, Juris
- Nature Communications, Vol. 11, Issue 1
Comparing proteins and nucleic acids for next-generation biomolecular engineering
journal, July 2018
- Pugh, Genevieve C.; Burns, Jonathan R.; Howorka, Stefan
- Nature Reviews Chemistry, Vol. 2, Issue 7
The multicatalytic compartment of propionyl-CoA synthase sequesters a toxic metabolite
journal, October 2018
- Bernhardsgrütter, Iria; Vögeli, Bastian; Wagner, Tristan
- Nature Chemical Biology, Vol. 14, Issue 12
SnoopLigase peptide-peptide conjugation enables modular vaccine assembly
journal, March 2019
- Andersson, Anne-Marie C.; Buldun, Can M.; Pattinson, David J.
- Scientific Reports, Vol. 9, Issue 1
Structural nanotechnology: three-dimensional cryo-EM and its use in the development of nanoplatforms for in vitro catalysis
journal, January 2019
- de Ruiter, Mark V.; Klem, Robin; Luque, Daniel
- Nanoscale, Vol. 11, Issue 10
Functional protein shells fabricated from the self-assembling protein sheets of prokaryotic organelles
journal, January 2020
- Bari, Naimat K.; Kumar, Gaurav; Hazra, Jagadish P.
- Journal of Materials Chemistry B, Vol. 8, Issue 3
Bio-engineering of bacterial microcompartments: a mini review
journal, June 2019
- Planamente, Sara; Frank, Stefanie
- Biochemical Society Transactions, Vol. 47, Issue 3
Structural and kinetic characterization of ( S )-1-amino-2-propanol kinase from the aminoacetone utilization microcompartment of Mycobacterium smegmatis
journal, October 2018
- Mallette, Evan; Kimber, Matthew S.
- Journal of Biological Chemistry, Vol. 293, Issue 51
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
- Ryan, Patrick; Forrester, Taylor J. B.; Wroblewski, Charles
- Journal of Biological Chemistry, Vol. 294, Issue 8
Fast normal mode computations of capsid dynamics inspired by resonance
journal, April 2018
- Na, Hyuntae; Song, Guang
- Physical Biology, Vol. 15, Issue 4
Symmetry considerations elucidate the roles of global shape and local interactions in the equilibrium fluctuations and cooperativity of protein assemblies
journal, April 2019
- Song, Guang
- Physical Biology, Vol. 16, Issue 4
Carboxysomes: metabolic modules for CO2 fixation
journal, August 2017
- Turmo, Aiko; Gonzalez-Esquer, C. Raul; Kerfeld, Cheryl A.
- FEMS Microbiology Letters, Vol. 364, Issue 18
Engineering the PduT shell protein to modify the permeability of the 1,2-propanediol microcompartment of Salmonella
journal, December 2019
- Chowdhury, Chiranjit; Bobik, Thomas A.
- Microbiology, Vol. 165, Issue 12
Harnessing the power of microbial nanowires
journal, May 2018
- Reguera, Gemma
- Microbial Biotechnology, Vol. 11, Issue 6
A Bacterial Microcompartment Is Used for Choline Fermentation by Escherichia coli 536
journal, March 2018
- Herring, Taylor I.; Harris, Tiffany N.; Chowdhury, Chiranjit
- Journal of Bacteriology, Vol. 200, Issue 10
Glycyl Radical Enzyme-Associated Microcompartments: Redox-Replete Bacterial Organelles
journal, January 2019
- Ferlez, Bryan; Sutter, Markus; Kerfeld, Cheryl A.
- mBio, Vol. 10, Issue 1
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
- Rohnke, Brandon A.; Singh, Shailendra P.; Pattanaik, Bagmi
- mSphere, Vol. 3, Issue 1
Self-Assembly Stability and Variability of Bacterial Microcompartment Shell Proteins in Response to the Environmental Change
journal, February 2019
- Faulkner, Matthew; Zhao, Long-Sheng; Barrett, Steve
- Nanoscale Research Letters, Vol. 14, Issue 1
Cellular origin of the viral capsid-like bacterial microcompartments
journal, November 2017
- Krupovic, Mart; Koonin, Eugene V.
- Biology Direct, Vol. 12, Issue 1
The role of the encapsulated cargo in microcompartment assembly
journal, July 2018
- Mohajerani, Farzaneh; Hagan, Michael F.
- PLOS Computational Biology, Vol. 14, Issue 7
All-atom normal mode dynamics of HIV-1 capsid
journal, September 2018
- Na, Hyuntae; Song, Guang
- PLOS Computational Biology, Vol. 14, Issue 9
Occurrence and stability of hetero-hexamer associations formed by β-carboxysome CcmK shell components
journal, October 2019
- Garcia-Alles, Luis F.; Root, Katharina; Maveyraud, Laurent
- PLOS ONE, Vol. 14, Issue 10
Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme
journal, January 2020
- Huang, Jingcheng; Ferlez, Bryan H.; Young, Eric J.
- Frontiers in Bioengineering and Biotechnology, Vol. 7
Comparative Genomic Analysis Reveals Novel Microcompartment-Associated Metabolic Pathways in the Human Gut Microbiome
journal, July 2019
- Ravcheev, Dmitry A.; Moussu, Lubin; Smajic, Semra
- Frontiers in Genetics, Vol. 10
Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications
journal, July 2017
- Young, Eric J.; Burton, Rodney; Mahalik, Jyoti P.
- Frontiers in Microbiology, Vol. 8