Structure and Function of a Bacterial Microcompartment Shell Protein Engineered to Bind a [4Fe-4S] Cluster (Journal Article) (original) (raw)

OSTI.GOV Journal Article: Structure and Function of a Bacterial Microcompartment Shell Protein Engineered to Bind a [4Fe-4S] Cluster

Journal Article · 24 Dec 2015 · Journal of the American Chemical Society

[Pandelia, Maria-Eirini [2]](/search/author:"Pandelia, Maria-Eirini"); [Sutter, Markus [3]](/search/author:"Sutter, Markus"); [Plegaria, Jefferson S. [1]](/search/author:"Plegaria, Jefferson S."); [Zarzycki, Jan [1]](/search/author:"Zarzycki, Jan"); [Turmo, Aiko [1]](/search/author:"Turmo, Aiko"); [Huang, Jingcheng [1]](/search/author:"Huang, Jingcheng"); [Ducat, Daniel C. [1]](/search/author:"Ducat, Daniel C."); [Hegg, Eric L. [4]](/search/author:"Hegg, Eric L."); [Gibney, Brian R. [5]](/search/author:"Gibney, Brian R."); [Kerfeld, Cheryl A. [6]](/search/author:"Kerfeld, Cheryl A.")

  1. Michigan State Univ., East Lansing, MI (United States). MSU DOE Plant Research Lab.
  2. Pennsylvania State Univ., University Park, PA (United States)
  3. Michigan State Univ., East Lansing, MI (United States). MSU DOE Plant Research Lab.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Michigan State Univ., East Lansing, MI (United States)
  5. Brooklyn College, Brooklyn, NY (United States)
  6. Michigan State Univ., East Lansing, MI (United States). MSU DOE Plant Research Lab.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States); Berkeley Synthetic Biology Inst., Berkeley, CA (United States)

Bacterial microcompartments (BMCs) are self-assembling organelles composed of a selectively permeable protein shell and encapsulated enzymes. They are considered promising templates for the engineering of designed bionanoreactors for biotechnology. In particular, encapsulation of oxidoreductive reactions requiring electron transfer between the lumen of the BMC and the cytosol relies on the ability to conduct electrons across the shell. We determined the crystal structure of a component protein of a synthetic BMC shell, which informed the rational design of a [4Fe-4S] cluster-binding site in its pore. Here, we also solved the structure of the [4Fe-4S] cluster-bound, engineered protein to 1.8 Å resolution, providing the first structure of a BMC shell protein containing a metal center. The [4Fe-4S] cluster was characterized by optical and EPR spectroscopies; it has a reduction potential of -370 mV vs the standard hydrogen electrode (SHE) and is stable through redox cycling. This remarkable stability may be attributable to the hydrogen-bonding network provided by the main chain of the protein scaffold. The properties of the [4Fe-4S] cluster resemble those in low-potential bacterial ferredoxins, while its ligation to three cysteine residues is reminiscent of enzymes such as aconitase and radical S-adenosymethionine (SAM) enzymes. This engineered shell protein provides the foundation for conferring electron-transfer functionality to BMC shells.

Research Organization:

Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

Sponsoring Organization:

USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:

FG02-91ER20021

OSTI ID:

1713208

Journal Information:

Journal of the American Chemical Society, Vol. 138, Issue 16; ISSN 0002-7863

Publisher:

American Chemical Society (ACS)Copyright Statement

Country of Publication:

United States

Language:

English

References (49)

Bacterial microcompartments and the modular construction of microbial metabolism Kerfeld, Cheryl A.; Erbilgin, Onur Trends in Microbiology, Vol. 23, Issue 1 https://doi.org/10.1016/j.tim.2014.10.003 journal January 2015
Ferrozine---a new spectrophotometric reagent for iron Stookey, Lawrence L. Analytical Chemistry, Vol. 42, Issue 7, p. 779-781 https://doi.org/10.1021/ac60289a016 journal June 1970
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
Structure and Properties of a Synthetic Analogue of Bacterial Iron-Sulfur Proteins Herskovitz, T.; Averill, B. A.; Holm, R. H. Proceedings of the National Academy of Sciences, Vol. 69, Issue 9 https://doi.org/10.1073/pnas.69.9.2437 journal September 1972
A De Novo Designed 2[4Fe-4S] Ferredoxin Mimic Mediates Electron Transfer Roy, Anindya; Sommer, Dayn Joseph; Schmitz, Robert Arthur Journal of the American Chemical Society, Vol. 136, Issue 49 https://doi.org/10.1021/ja510621e journal November 2014
Iron-Sulfur Clusters: Nature's Modular, Multipurpose Structures Beinert, H. Science, Vol. 277, Issue 5326 https://doi.org/10.1126/science.277.5326.653 journal August 1997
The rational design and construction of a cuboidal iron-sulfur protein Coldren, C. D.; Hellinga, H. W.; Caradonna, J. P. Proceedings of the National Academy of Sciences, Vol. 94, Issue 13 https://doi.org/10.1073/pnas.94.13.6635 journal June 1997
High-Yield Expression of Heterologous [FeFe] Hydrogenases in Escherichia coli Kuchenreuther, Jon M.; Grady-Smith, Celestine S.; Bingham, Alyssa S. PLoS ONE, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pone.0015491 journal November 2010
Femtomolar Zn(II) Affinity in a Peptide-Based Ligand Designed To Model Thiolate-Rich Metalloprotein Active Sites Petros, Amy K.; Reddi, Amit R.; Kennedy, Michelle L. Inorganic Chemistry, Vol. 45, Issue 25 https://doi.org/10.1021/ic052190q journal December 2006
De Novo Design of a Redox-Active Minimal Rubredoxin Mimic Nanda, Vikas; Rosenblatt, Michael M.; Osyczka, Artur Journal of the American Chemical Society, Vol. 127, Issue 16 https://doi.org/10.1021/ja050553f journal April 2005
Insight into the protein and solvent contributions to the reduction potentials of [4Fe–4S]2+/+ clusters: crystal structures of the Allochromatium vinosum ferredoxin variants C57A and V13G and the homologous Escherichia coli ferredoxin Saridakis, Emmanuel; Giastas, Petros; Efthymiou, Georgios JBIC Journal of Biological Inorganic Chemistry, Vol. 14, Issue 5 https://doi.org/10.1007/s00775-009-0492-x journal March 2009
Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins: Pentameric Structure of a Shell Protein from a Grp Microcompartment Wheatley, Nicole M.; Gidaniyan, Soheil D.; Liu, Yuxi Protein Science, Vol. 22, Issue 5 https://doi.org/10.1002/pro.2246 journal April 2013
Ferredoxin and ferredoxin-heme maquettes Gibney, B. R.; Mulholland, S. E.; Rabanal, F. Proceedings of the National Academy of Sciences, Vol. 93, Issue 26 https://doi.org/10.1073/pnas.93.26.15041 journal December 1996
The structure of the 2[4Fe–4S] ferredoxin from Pseudomonas aeruginosa at 1.32-Å resolution: comparison with other high-resolution structures of ferredoxins and contributing structural features to reduction potential values Giastas, Petros; Pinotsis, Nikos; Efthymiou, Georgios JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 4 https://doi.org/10.1007/s00775-006-0094-9 journal April 2006
A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method Axen, Seth D.; Erbilgin, Onur; Kerfeld, Cheryl A. PLoS Computational Biology, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pcbi.1003898 journal October 2014
Short N-terminal sequences package proteins into bacterial microcompartments Fan, C.; Cheng, S.; Liu, Y. Proceedings of the National Academy of Sciences, Vol. 107, Issue 16 https://doi.org/10.1073/pnas.0913199107 journal March 2010
[Fe4S4]- and [Fe3S4]-cluster formation in synthetic peptides Hoppe, Alessandra; Pandelia, Maria-Eirini; Gärtner, Wolfgang Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 11 https://doi.org/10.1016/j.bbabio.2011.06.017 journal November 2011
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
Biochemical and Structural Insights into Bacterial Organelle Form and Biogenesis Parsons, Joshua B.; Dinesh, Sriramulu D.; Deery, Evelyne Journal of Biological Chemistry, Vol. 283, Issue 21 https://doi.org/10.1074/jbc.M709214200 journal March 2008
Atomic-Level Models of the Bacterial Carboxysome Shell Tanaka, S.; Kerfeld, C. A.; Sawaya, M. R. Science, Vol. 319, Issue 5866 https://doi.org/10.1126/science.1151458 journal February 2008
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337 journal January 2010
The Redox Potential of Dithionite and SO-2 from Equilibrium Reactions with Flavodoxins, Methyl Viologen and Hydrogen plus Hydrogenase Mayhew, Stephen G. European Journal of Biochemistry, Vol. 85, Issue 2 https://doi.org/10.1111/j.1432-1033.1978.tb12269.x journal April 1978
Identification of a Unique Fe-S Cluster Binding Site in a Glycyl-Radical Type Microcompartment Shell Protein Thompson, Michael C.; Wheatley, Nicole M.; Jorda, Julien Journal of Molecular Biology, Vol. 426, Issue 19 https://doi.org/10.1016/j.jmb.2014.07.018 journal September 2014
Structure of activated aconitase: formation of the [4Fe-4S] cluster in the crystal. Robbins, A. H.; Stout, C. D. Proceedings of the National Academy of Sciences, Vol. 86, Issue 10 https://doi.org/10.1073/pnas.86.10.3639 journal May 1989
Radical S -Adenosylmethionine Enzymes Broderick, Joan B.; Duffus, Benjamin R.; Duschene, Kaitlin S. Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4004709 journal January 2014
Iron-sulfur clusters: ever-expanding roles Fontecave, Marc Nature Chemical Biology, Vol. 2, Issue 4 https://doi.org/10.1038/nchembio0406-171 journal April 2006
Redox potentiometry: Determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems Leslie Dutton, P. Methods in Enzymology https://doi.org/10.1016/S0076-6879(78)54026-3 book January 1978
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
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
Proteins Containing 4Fe-4S Clusters: An Overview Sweeney, W. V.; Rabinowitz, J. C. Annual Review of Biochemistry, Vol. 49, Issue 1 https://doi.org/10.1146/annurev.bi.49.070180.001035 journal June 1980
Dithiothreitol, a New Protective Reagent for SH Groups * Cleland, W. W. Biochemistry, Vol. 3, Issue 4 https://doi.org/10.1021/bi00892a002 journal April 1964
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925 journal January 2010
Characterization of [4Fe-4S] Cluster Vibrations and Structure in Nitrogenase Fe Protein at Three Oxidation Levels via Combined NRVS, EXAFS, and DFT Analyses Mitra, Devrani; George, Simon J.; Guo, Yisong Journal of the American Chemical Society, Vol. 135, Issue 7 https://doi.org/10.1021/ja307027n journal February 2013
Synthesis and characterization of de novo designed peptides modelling the binding sites of [4Fe–4S] clusters in photosystem I Antonkine, Mikhail L.; Koay, Melissa S.; Epel, Boris Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 8 https://doi.org/10.1016/j.bbabio.2009.03.007 journal August 2009
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
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
Solution Structure of a Bacterial Microcompartment Targeting Peptide and Its Application in the Construction of an Ethanol Bioreactor Lawrence, Andrew D.; Frank, Stefanie; Newnham, Sarah ACS Synthetic Biology, Vol. 3, Issue 7 https://doi.org/10.1021/sb4001118 journal November 2013
Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways: Bacterial microcompartments Bobik, Thomas A.; Lehman, Brent P.; Yeates, Todd O. Molecular Microbiology, Vol. 98, Issue 2 https://doi.org/10.1111/mmi.13117 journal August 2015
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
Two new high-resolution crystal structures of carboxysome pentamer proteins reveal high structural conservation of CcmL orthologs among distantly related cyanobacterial species Sutter, Markus; Wilson, Steven C.; Deutsch, Samuel Photosynthesis Research, Vol. 118, Issue 1-2 https://doi.org/10.1007/s11120-013-9909-z journal August 2013
Comparative analysis of carboxysome shell proteins Kinney, James N.; Axen, Seth D.; Kerfeld, Cheryl A. Photosynthesis Research, Vol. 109, Issue 1-3 https://doi.org/10.1007/s11120-011-9624-6 journal January 2011
Protein Design: Toward Functional Metalloenzymes Yu, Fangting; Cangelosi, Virginia M.; Zastrow, Melissa L. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr400458x journal January 2014
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013 journal January 2006
De novo design of a non-natural fold for an iron–sulfur protein: Alpha-helical coiled-coil with a four-iron four-sulfur cluster binding site in its central core Grzyb, Joanna; Xu, Fei; Weiner, Lev Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 3 https://doi.org/10.1016/j.bbabio.2009.12.012 journal March 2010
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
Iron-sulphur clusters and the problem with oxygen Imlay, James A. Molecular Microbiology, Vol. 59, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05028.x journal February 2006
Protein Structures Forming the Shell of Primitive Bacterial Organelles Kerfeld, C. A. Science, Vol. 309, Issue 5736 https://doi.org/10.1126/science.1113397 journal August 2005
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206 journal July 2007
RlmN and AtsB as Models for the Overproduction and Characterization of Radical SAM Proteins Lanz, Nicholas D.; Grove, Tyler L.; Gogonea, Camelia Baleanu Methods in Enzymology https://doi.org/10.1016/B978-0-12-394291-3.00030-7 book January 2012

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Bacterial Microcompartments Kerfeld, Cheryl A.; Heinhorst, Sabine; Cannon, Gordon C. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.112408.134211 journal October 2010
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