skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme

; ; ; ; ;
Publication Date:
Sponsoring Org.:
OSTI Identifier:
Resource Type:
Published Article
Journal Name:
Frontiers in Bioengineering and Biotechnology
Additional Journal Information:
Journal Name: Frontiers in Bioengineering and Biotechnology Journal Volume: 7; Journal ID: ISSN 2296-4185
Frontiers Media SA
Country of Publication:

Citation Formats

Huang, Jingcheng, Ferlez, Bryan H., Young, Eric J., Kerfeld, Cheryl A., Kramer, David M., and Ducat, Daniel C. Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme. Switzerland: N. p., 2020. Web. doi:10.3389/fbioe.2019.00432.
Huang, Jingcheng, Ferlez, Bryan H., Young, Eric J., Kerfeld, Cheryl A., Kramer, David M., & Ducat, Daniel C. Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme. Switzerland. doi:10.3389/fbioe.2019.00432.
Huang, Jingcheng, Ferlez, Bryan H., Young, Eric J., Kerfeld, Cheryl A., Kramer, David M., and Ducat, Daniel C. Thu . "Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme". Switzerland. doi:10.3389/fbioe.2019.00432.
title = {Functionalization of Bacterial Microcompartment Shell Proteins With Covalently Attached Heme},
author = {Huang, Jingcheng and Ferlez, Bryan H. and Young, Eric J. and Kerfeld, Cheryl A. and Kramer, David M. and Ducat, Daniel C.},
abstractNote = {},
doi = {10.3389/fbioe.2019.00432},
journal = {Frontiers in Bioengineering and Biotechnology},
number = ,
volume = 7,
place = {Switzerland},
year = {2020},
month = {1}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.3389/fbioe.2019.00432

Save / Share:

Works referenced in this record:

Control of Cytochrome c Redox Potential:  Axial Ligation and Protein Environment Effects
journal, May 2002

  • Battistuzzi, Gianantonio; Borsari, Marco; Cowan, James A.
  • Journal of the American Chemical Society, Vol. 124, Issue 19
  • DOI: 10.1021/ja017479v

The Plasticity of Molecular Interactions Governs Bacterial Microcompartment Shell Assembly
journal, May 2019

Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications
journal, July 2017

What is the substrate specificity of the System I cytochrome c biogenesis apparatus?
journal, January 2006

  • Allen, J. W. A.; Ferguson, S. J.
  • Biochemical Society Transactions, Vol. 34, Issue 1
  • DOI: 10.1042/BST0340150

Post-Crystal Engineering of Zinc-Substituted Myoglobin to Construct a Long-Lived Photoinduced Charge-Separation System
journal, April 2011

  • Koshiyama, Tomomi; Shirai, Masanobu; Hikage, Tatsuo
  • Angewandte Chemie International Edition, Vol. 50, Issue 21
  • DOI: 10.1002/anie.201008004

Multilevel Biomemory Device Consisting of Recombinant Azurin/Cytochrome c
journal, January 2010

Escherichia coli genes required for cytochrome c maturation.
journal, August 1995

Design and synthesis of multi-haem proteins
journal, March 1994

  • Robertson, Dan E.; Farid, Ramy S.; Moser, Christopher C.
  • Nature, Vol. 368, Issue 6470, p. 425-432
  • DOI: 10.1038/368425a0

CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data
journal, July 2013

  • Huang, Jing; MacKerell, Alexander D.
  • Journal of Computational Chemistry, Vol. 34, Issue 25
  • DOI: 10.1002/jcc.23354

A non-compartmentalized glucose∣O2 biofuel cell by bioengineered electrode surfaces
journal, December 1999

  • Katz, Eugenii; Willner, Itamar; Kotlyar, Alexander B.
  • Journal of Electroanalytical Chemistry, Vol. 479, Issue 1
  • DOI: 10.1016/S0022-0728(99)00425-8

Structure of the Type IVa Major Pilin from the Electrically Conductive Bacterial Nanowires of Geobacter sulfurreducens
journal, August 2013

  • Reardon, Patrick N.; Mueller, Karl T.
  • Journal of Biological Chemistry, Vol. 288, Issue 41
  • DOI: 10.1074/jbc.M113.498527

Overproduction of theBradyrhizobium japonicum c-Type Cytochrome Subunits of thecbb3Oxidase inEscherichia coli
journal, October 1998

  • Arslan, Engin; Schulz, Henk; Zufferey, Rachel
  • Biochemical and Biophysical Research Communications, Vol. 251, Issue 3
  • DOI: 10.1006/bbrc.1998.9549

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Purification and Characterization of Protein Nanotubes Assembled from a Single Bacterial Microcompartment Shell Subunit
journal, October 2015

  • Noël, Christopher R.; Cai, Fei; Kerfeld, Cheryl A.
  • Advanced Materials Interfaces, Vol. 3, Issue 1
  • DOI: 10.1002/admi.201500295

Protein bioelectronics: a review of what we do and do not know
journal, January 2018

  • Bostick, Christopher D.; Mukhopadhyay, Sabyasachi; Pecht, Israel
  • Reports on Progress in Physics, Vol. 81, Issue 2
  • DOI: 10.1088/1361-6633/aa85f2

Natural engineering principles of electron tunnelling in biological oxidation–reduction
journal, November 1999

  • Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi
  • Nature, Vol. 402, Issue 6757
  • DOI: 10.1038/46972

Heme Protein Assemblies
journal, February 2004

  • Reedy, Charles J.; Gibney, Brian R.
  • Chemical Reviews, Vol. 104, Issue 2
  • DOI: 10.1021/cr0206115

Protein electron transfer: Dynamics and statistics
journal, July 2013

  • Matyushov, Dmitry V.
  • The Journal of Chemical Physics, Vol. 139, Issue 2
  • DOI: 10.1063/1.4812788

Structure of a novel 13 nm dodecahedral nanocage assembled from a redesigned bacterial microcompartment shell protein
journal, January 2016

  • Jorda, J.; Leibly, D. J.; Thompson, M. C.
  • Chemical Communications, Vol. 52, Issue 28
  • DOI: 10.1039/c6cc00851h

Nano-hemoglobin film based sextet state biomemory device by cross-linked photosensitive hapten monomer
journal, January 2018

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
  • DOI: 10.1021/jacs.5b11734

A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method
journal, October 2014

A spectroelectrochemical study of microperoxidase at bare and gold-plated RVC thin-layer electrodes
journal, June 1990

  • Zamponi, Silvia; Santucci, Roberto; Brunori, Maurizio
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1034, Issue 3
  • DOI: 10.1016/0304-4165(90)90054-z

Structural Insights into Higher Order Assembly and Function of the Bacterial Microcompartment Protein PduA
journal, May 2014

  • Pang, Allan; Frank, Stefanie; Brown, Ian
  • Journal of Biological Chemistry, Vol. 289, Issue 32
  • DOI: 10.1074/jbc.M114.569285

Photoinduced charge separation in single-walled carbon nanotube/protein integrated systems
journal, January 2017

  • Kubie, Lenore; Amori, Amanda R.; Chakraborty, Saikat
  • Nanoscale Horizons, Vol. 2, Issue 3
  • DOI: 10.1039/C6NH00172F

Site-directed mutageneses of rat liver cytochrome P-450d: axial ligand and heme incorporation
journal, May 1988

  • Shimizu, Toru; Hirano, Kenji; Takahashi, Masae
  • Biochemistry, Vol. 27, Issue 11
  • DOI: 10.1021/bi00411a035

Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell
journal, June 2017

Ligand preference and orientation in b- and c-type heme-binding proteins
journal, May 2008

  • Fufezan, Christian; Zhang, Jun; Gunner, M. R.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 73, Issue 3
  • DOI: 10.1002/prot.22097

Bacterial microcompartments
journal, March 2018

  • Kerfeld, Cheryl A.; Aussignargues, Clement; Zarzycki, Jan
  • Nature Reviews Microbiology, Vol. 16, Issue 5
  • DOI: 10.1038/nrmicro.2018.10

Visualization of Bacterial Microcompartment Facet Assembly Using High-Speed Atomic Force Microscopy
journal, December 2015

Engineering nanoreactors using bacterial microcompartment architectures
journal, June 2018

A synthetic redox biofilm made from metalloprotein–prion domain chimera nanowires
journal, October 2016

  • Altamura, Lucie; Horvath, Christophe; Rengaraj, Saravanan
  • Nature Chemistry, Vol. 9, Issue 2
  • DOI: 10.1038/nchem.2616

Programmed loading and rapid purification of engineered bacterial microcompartment shells
journal, July 2018

Identification of a Unique Fe-S Cluster Binding Site in a Glycyl-Radical Type Microcompartment Shell Protein
journal, September 2014

  • Thompson, Michael C.; Wheatley, Nicole M.; Jorda, Julien
  • Journal of Molecular Biology, Vol. 426, Issue 19
  • DOI: 10.1016/j.jmb.2014.07.018

Constructing a man-made c-type cytochrome maquette in vivo: electron transfer, oxygen transport and conversion to a photoactive light harvesting maquette.
journal, January 2014

  • Anderson, J. L. Ross; Armstrong, Craig T.; Kodali, Goutham
  • Chem. Sci., Vol. 5, Issue 2
  • DOI: 10.1039/C3SC52019F

Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway
journal, November 2013

Hydrogen evolution from water catalyzed by cobalt-mimochrome VI*a, a synthetic mini-protein
journal, January 2018

  • Firpo, Vincenzo; Le, Jennifer M.; Pavone, Vincenzo
  • Chemical Science, Vol. 9, Issue 45
  • DOI: 10.1039/c8sc01948g

Design and Synthesis of a Globin Fold †
journal, June 1999

  • Isogai, Yasuhiro; Ota, Motonori; Fujisawa, Tetsuro
  • Biochemistry, Vol. 38, Issue 23
  • DOI: 10.1021/bi983006y

Hemoproteins in Design of Biofuel Cells
journal, February 2009

Geometrical Description of Protein Structural Motifs
journal, August 2018

  • Kozak, John J.; Gray, Harry B.; Wittung-Stafshede, Pernilla
  • The Journal of Physical Chemistry B, Vol. 122, Issue 49
  • DOI: 10.1021/acs.jpcb.8b07130

Miniaturized hemoproteins: design, synthesis and characterization of mimochrome II
journal, July 1998

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
  • DOI: 10.1080/19420889.2015.1039755

Geometric constraints for porphyrin binding in helical protein binding sites
journal, February 2009

  • Negron, Christopher; Fufezan, Christian; Koder, Ronald L.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 74, Issue 2
  • DOI: 10.1002/prot.22143

Amino acid-substituted iron porphyrins. 2. Thermodynamic studies of ligand binding
journal, September 1976

In Vitro Assembly of Diverse Bacterial Microcompartment Shell Architectures
journal, October 2018

Crystal Structures at Atomic Resolution Reveal the Novel Concept of “Electron-harvesting” as a Role for the Small Tetraheme Cytochrome c
journal, June 2002

  • Leys, David; Meyer, Terrance E.; Tsapin, Alexandre S.
  • Journal of Biological Chemistry, Vol. 277, Issue 38
  • DOI: 10.1074/jbc.M203866200

Hydrogen Evolution from Neutral Water under Aerobic Conditions Catalyzed by Cobalt Microperoxidase-11
journal, December 2013

  • Kleingardner, Jesse G.; Kandemir, Banu; Bren, Kara L.
  • Journal of the American Chemical Society, Vol. 136, Issue 1
  • DOI: 10.1021/ja406818h

The Reorganization Energy in Cytochrome c is Controlled by the Accessibility of the Heme to the Solvent
journal, June 2011

  • Bortolotti, Carlo Augusto; Siwko, Magdalena E.; Castellini, Elena
  • The Journal of Physical Chemistry Letters, Vol. 2, Issue 14
  • DOI: 10.1021/jz200734a

Design, Synthesis, and Circular Dichroism Investigation of a Peptide-Sandwiched Mesoheme
journal, August 1995

  • Benson, David R.; Hart, Bradley R.; Zhu, Xiao
  • Journal of the American Chemical Society, Vol. 117, Issue 33
  • DOI: 10.1021/ja00138a002

Bio-engineering of bacterial microcompartments: a mini review
journal, June 2019

  • Planamente, Sara; Frank, Stefanie
  • Biochemical Society Transactions, Vol. 47, Issue 3
  • DOI: 10.1042/BST20170564

Peptide-Based Heme−Protein Models
journal, October 2001

  • Lombardi, Angela; Nastri, Flavia; Pavone, Vincenzo
  • Chemical Reviews, Vol. 101, Issue 10
  • DOI: 10.1021/cr000055j

Bacterial microcompartments: their properties and paradoxes
journal, November 2008

  • Cheng, Shouqiang; Liu, Yu; Crowley, Christopher S.
  • BioEssays, Vol. 30, Issue 11-12
  • DOI: 10.1002/bies.20830

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

Encapsulation of multiple cargo proteins within recombinant Eut nanocompartments
journal, July 2016

  • Quin, Maureen B.; Perdue, Sarah A.; Hsu, Szu-Yi
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 21
  • DOI: 10.1007/s00253-016-7737-8

A Superoxide Sensor Based on a Multilayer Cytochrome c Electrode
journal, August 2004

  • Beissenhirtz, Moritz K.; Scheller, Frieder W.; Lisdat, Fred
  • Analytical Chemistry, Vol. 76, Issue 16
  • DOI: 10.1021/ac049738f

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
  • DOI: 10.1038/nchembio.2535

Diffusionless electron transfer of microperoxidase-11 on gold electrodes
journal, July 1999

A designed bacterial microcompartment shell with tunable composition and precision cargo loading
journal, July 2019

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
  • Journal of Molecular Biology, Vol. 426, Issue 12
  • DOI: 10.1016/j.jmb.2014.04.012

SWISS-MODEL: homology modelling of protein structures and complexes
journal, May 2018

  • Waterhouse, Andrew; Bertoni, Martino; Bienert, Stefan
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky427

The chemistry and biochemistry of heme c: functional bases for covalent attachment
journal, January 2008

  • Bowman, Sarah E. J.; Bren, Kara L.
  • Natural Product Reports, Vol. 25, Issue 6
  • DOI: 10.1039/b717196j

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
  • DOI: 10.1016/j.jmb.2014.02.025

Microperoxidase 11: a model system for porphyrin networks and heme–protein interactions
journal, July 2009

  • Verbaro, Daniel; Hagarman, Andrew; Kohli, Ajay
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 14, Issue 8
  • DOI: 10.1007/s00775-009-0574-9

Structural analysis of heme proteins: implications for design and prediction
journal, January 2011

  • Li, Ting; Bonkovsky, Herbert L.; Guo, Jun-tao
  • BMC Structural Biology, Vol. 11, Issue 1
  • DOI: 10.1186/1472-6807-11-13

A heme tag for in vivo synthesis of artificial cytochromes
journal, December 2004

  • Braun, Martin; Rubio, In�s Garc�a; Th�ny-Meyer, Linda
  • Applied Microbiology and Biotechnology, Vol. 67, Issue 2
  • DOI: 10.1007/s00253-004-1804-2

Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O 2
journal, January 2012

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
  • DOI: 10.1016/j.jmb.2009.03.056

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
  • DOI: 10.1074/jbc.M116.754093

An allosteric model for control of pore opening by substrate binding in the EutL microcompartment shell protein: Pore Regulation by Substrate Binding
journal, March 2015

  • Thompson, Michael C.; Cascio, Duilio; Leibly, David J.
  • Protein Science, Vol. 24, Issue 6
  • DOI: 10.1002/pro.2672

VMD: Visual molecular dynamics
journal, February 1996

Protein Structures Forming the Shell of Primitive Bacterial Organelles
journal, August 2005

A Generic Self-Assembly Process in Microcompartments and Synthetic Protein Nanotubes
journal, March 2018