Structural Characterization of a Synthetic Tandem-Domain Bacterial Microcompartment Shell Protein Capable of Forming Icosahedral Shell Assemblies

Sutter, Markus; McGuire, Sean; Ferlez, Bryan; Kerfeld, Cheryl A.

doi:10.1021/acssynbio.9b00011

Title: Structural Characterization of a Synthetic Tandem-Domain Bacterial Microcompartment Shell Protein Capable of Forming Icosahedral Shell Assemblies

Journal Article · Fri Mar 22 00:00:00 EDT 2019 · ACS Synthetic Biology

DOI:https://doi.org/10.1021/acssynbio.9b00011· OSTI ID:1671311

Sutter, Markus ^[1]; McGuire, Sean ^[2];

^[2];

^[1]

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Michigan State University, East Lansing, MI (United States)
Michigan State University, East Lansing, MI (United States)

Bacterial microcompartments are subcellular compartments found in many prokaryotes; they consist of a protein shell that encapsulates enzymes that perform a variety of functions. The shell protects the cell from potentially toxic intermediates and co-localizes enzymes for higher efficiency. Accordingly, it is of considerable interest for biotechnological applications. We have previously structurally characterized an intact 40 nm shell comprised of three different types of proteins. One of those proteins, BMC-H, forms a cyclic hexamer; here we have engineered a synthetic protein that consists of a tandem duplication of BMC-H connected by a short linker. The synthetic protein forms cyclic trimers that self-assemble to form a smaller (25 nm) icosahedral shell with gaps at the pentamer positions. When co-expressed in vivo with the pentamer fused to an affinity tag we can purify complete icosahedral shells. This engineered shell protein constitutes a minimal shell system to study permeability; reducing symmetry from six- to three-fold will allow for finer control of the pore environment. In conclusion, we have determined a crystal structure of this shell to guide rational engineering of this microcompartment shell for biotechnological applications.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID)

Grant/Contract Number:: FG02-91ER20021; 1R01AI114975-01; AC02-05CH11231

OSTI ID:: 1671311

Journal Information:: ACS Synthetic Biology, Vol. 8, Issue 4; ISSN 2161-5063

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (30)

Bacterial microcompartments Kerfeld, Cheryl A.; Aussignargues, Clement; Zarzycki, Jan Nature Reviews Microbiology, Vol. 16, Issue 5 https://doi.org/10.1038/nrmicro.2018.10	journal	March 2018
Bacterial microcompartments moving into a synthetic biological world Frank, Stefanie; Lawrence, Andrew D.; Prentice, Michael B. Journal of Biotechnology, Vol. 163, Issue 2 https://doi.org/10.1016/j.jbiotec.2012.09.002	journal	January 2013
Assembly of Robust Bacterial Microcompartment Shells Using Building Blocks from an Organelle of Unknown Function Lassila, Jonathan K.; Bernstein, Susan L.; Kinney, James N. Journal of Molecular Biology, Vol. 426, Issue 11 https://doi.org/10.1016/j.jmb.2014.02.025	journal	May 2014
Bacterial microcompartment-directed polyphosphate kinase promotes stable polyphosphate accumulation in E. coli Liang, Mingzhi; Frank, Stefanie; Lünsdorf, Heinrich Biotechnology Journal, Vol. 12, Issue 3 https://doi.org/10.1002/biot.201600415	journal	February 2017
Characterisation of PduS, the pdu Metabolosome Corrin Reductase, and Evidence of Substructural Organisation within the Bacterial Microcompartment Parsons, Joshua B.; Lawrence, Andrew D.; McLean, Kirsty J. PLoS ONE, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pone.0014009	journal	November 2010
Gene fusion/fission is a major contributor to evolution of multi-domain bacterial proteins Pasek, S.; Risler, J. -L.; Brezellec, P. Bioinformatics, Vol. 22, Issue 12 https://doi.org/10.1093/bioinformatics/btl135	journal	April 2006
Structure, function and evolution of multidomain proteins Vogel, Christine; Bashton, Matthew; Kerrison, Nicola D. Current Opinion in Structural Biology, Vol. 14, Issue 2 https://doi.org/10.1016/j.sbi.2004.03.011	journal	April 2004
Role of selection in fixation of gene duplications Kondrashov, Fyodor A.; Kondrashov, Alexey S. Journal of Theoretical Biology, Vol. 239, Issue 2 https://doi.org/10.1016/j.jtbi.2005.08.033	journal	March 2006
Functional innovation from changes in protein domains and their combinations Lees, Jonathan G.; Dawson, Natalie L.; Sillitoe, Ian Current Opinion in Structural Biology, Vol. 38 https://doi.org/10.1016/j.sbi.2016.05.016	journal	June 2016
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport Klein, Michael G.; Zwart, Peter; Bagby, Sarah C. Journal of Molecular Biology, Vol. 392, Issue 2 https://doi.org/10.1016/j.jmb.2009.03.056	journal	September 2009
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment Cai, Fei; Sutter, Markus; Cameron, Jeffrey C. Journal of Biological Chemistry, Vol. 288, Issue 22 https://doi.org/10.1074/jbc.M113.456897	journal	April 2013
Crystallographic Insights into the Pore Structures and Mechanisms of the EutL and EutM Shell Proteins of the Ethanolamine-Utilizing Microcompartment of Escherichia coli Takenoya, M.; Nikolakakis, K.; Sagermann, M. Journal of Bacteriology, Vol. 192, Issue 22 https://doi.org/10.1128/JB.00652-10	journal	September 2010
Structure of a trimeric bacterial microcompartment shell protein, EtuB, associated with ethanol utilization in Clostridium kluyveri Heldt, Dana; Frank, Stefanie; Seyedarabi, Arefeh Biochemical Journal, Vol. 423, Issue 2 https://doi.org/10.1042/BJ20090780	journal	September 2009
Crystal structure of the EutL shell protein of the ethanolamine ammonia lyase microcompartment Sagermann, M.; Ohtaki, A.; Nikolakakis, K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 22 https://doi.org/10.1073/pnas.0902324106	journal	May 2009
Structure of PduT, a trimeric bacterial microcompartment protein with a 4Fe–4S cluster-binding site Pang, Allan; Warren, Martin J.; Pickersgill, Richard W. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 2 https://doi.org/10.1107/S0907444910050201	journal	January 2011
Structural Insight into the Mechanisms of Transport across the Salmonella enterica Pdu Microcompartment Shell Crowley, Christopher S.; Cascio, Duilio; Sawaya, Michael R. Journal of Biological Chemistry, Vol. 285, Issue 48 https://doi.org/10.1074/jbc.M110.160580	journal	September 2010
Programmed loading and rapid purification of engineered bacterial microcompartment shells Hagen, Andrew; Sutter, Markus; Sloan, Nancy Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05162-z	journal	July 2018
Structure and Function of a Bacterial Microcompartment Shell Protein Engineered to Bind a [4Fe-4S] Cluster Aussignargues, Clément; Pandelia, Maria-Eirini; Sutter, Markus Journal of the American Chemical Society, Vol. 138, Issue 16 https://doi.org/10.1021/jacs.5b11734	journal	January 2016
Visualization of Bacterial Microcompartment Facet Assembly Using High-Speed Atomic Force Microscopy Sutter, Markus; Faulkner, Matthew; Aussignargues, Clément Nano Letters, Vol. 16, Issue 3 https://doi.org/10.1021/acs.nanolett.5b04259	journal	December 2015
In Vitro Assembly of Diverse Bacterial Microcompartment Shell Architectures Hagen, Andrew R.; Plegaria, Jefferson S.; Sloan, Nancy Nano Letters, Vol. 18, Issue 11 https://doi.org/10.1021/acs.nanolett.8b02991	journal	October 2018
Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell Sutter, Markus; Greber, Basil; Aussignargues, Clement Science, Vol. 356, Issue 6344 https://doi.org/10.1126/science.aan3289	journal	June 2017
What stabilizes close arginine pairing in proteins? Lee, Dongseon; Lee, Juyong; Seok, Chaok Physical Chemistry Chemical Physics, Vol. 15, Issue 16 https://doi.org/10.1039/c3cp00160a	journal	January 2013
Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome Tsai, Yingssu; Sawaya, Michael R.; Cannon, Gordon C. PLoS Biology, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pbio.0050144	journal	May 2007
Engineered Protein Nano-Compartments for Targeted Enzyme Localization Choudhary, Swati; Quin, Maureen B.; Sanders, Mark A. PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033342	journal	March 2012
Structural basis of enzyme encapsulation into a bacterial nanocompartment Sutter, Markus; Boehringer, Daniel; Gutmann, Sascha Nature Structural & Molecular Biology, Vol. 15, Issue 9 https://doi.org/10.1038/nsmb.1473	journal	August 2008
Encapsulins: molecular biology of the shell Nichols, Robert J.; Cassidy-Amstutz, Caleb; Chaijarasphong, Thawatchai Critical Reviews in Biochemistry and Molecular Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10409238.2017.1337709	journal	June 2017
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004

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59 BASIC BIOLOGICAL SCIENCES
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size exclusion chromatography
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crystal structure
mathematical methods

Title: Structural Characterization of a Synthetic Tandem-Domain Bacterial Microcompartment Shell Protein Capable of Forming Icosahedral Shell Assemblies

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