The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene
Abstract
Bacterial microcompartments (MCPs) are complex organelles that consist of metabolic enzymes encapsulated within a protein shell. Here, we investigate the function of the PduJ MCP shell protein. PduJ is 80% identical in amino acid sequence to PduA and both are major shell proteins of the 1,2-propanediol (1,2-PD) utilization (Pdu) MCP of Salmonella. Prior studies showed that PduA mediates the transport of 1,2-PD (the substrate) into the Pdu MCP. Surprisingly, however, results presented here establish that PduJ has no role 1,2-PD transport. The crystal structure revealed that PduJ was nearly identical to that of PduA and, hence, offered no explanation for their differential functions. Interestingly, however, when a pduJ gene was placed at the pduA chromosomal locus, the PduJ protein acquired a new function, the ability to mediate 1,2-PD transport into the Pdu MCP. To our knowledge, these are the first studies to show that that gene location can determine the function of a MCP shell protein. We propose that gene location dictates protein-protein interactions essential to the function of the MCP shell.
- Authors:
-
- Iowa State Univ., Ames, IA (United States)
- Univ. of California, Los Angeles, CA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Center for Research Resources; National Institute of General Medical Sciences (NIGMS)
- OSTI Identifier:
- 1328044
- Grant/Contract Number:
- R01AI081146; T32-GM008496; 5P41RR015301-10; 8 P41 GM103403-10; AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Microbiology
- Additional Journal Information:
- Journal Volume: 101; Journal Issue: 5; Journal ID: ISSN 0950-382X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Chowdhury, Chiranjit, Chun, Sunny, Sawaya, Michael R., Yeates, Todd O., and Bobik, Thomas A. The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene. United States: N. p., 2016.
Web. doi:10.1111/mmi.13423.
Chowdhury, Chiranjit, Chun, Sunny, Sawaya, Michael R., Yeates, Todd O., & Bobik, Thomas A. The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene. United States. https://doi.org/10.1111/mmi.13423
Chowdhury, Chiranjit, Chun, Sunny, Sawaya, Michael R., Yeates, Todd O., and Bobik, Thomas A. Tue .
"The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene". United States. https://doi.org/10.1111/mmi.13423. https://www.osti.gov/servlets/purl/1328044.
@article{osti_1328044,
title = {The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene},
author = {Chowdhury, Chiranjit and Chun, Sunny and Sawaya, Michael R. and Yeates, Todd O. and Bobik, Thomas A.},
abstractNote = {Bacterial microcompartments (MCPs) are complex organelles that consist of metabolic enzymes encapsulated within a protein shell. Here, we investigate the function of the PduJ MCP shell protein. PduJ is 80% identical in amino acid sequence to PduA and both are major shell proteins of the 1,2-propanediol (1,2-PD) utilization (Pdu) MCP of Salmonella. Prior studies showed that PduA mediates the transport of 1,2-PD (the substrate) into the Pdu MCP. Surprisingly, however, results presented here establish that PduJ has no role 1,2-PD transport. The crystal structure revealed that PduJ was nearly identical to that of PduA and, hence, offered no explanation for their differential functions. Interestingly, however, when a pduJ gene was placed at the pduA chromosomal locus, the PduJ protein acquired a new function, the ability to mediate 1,2-PD transport into the Pdu MCP. To our knowledge, these are the first studies to show that that gene location can determine the function of a MCP shell protein. We propose that gene location dictates protein-protein interactions essential to the function of the MCP shell.},
doi = {10.1111/mmi.13423},
journal = {Molecular Microbiology},
number = 5,
volume = 101,
place = {United States},
year = {Tue Jun 07 00:00:00 EDT 2016},
month = {Tue Jun 07 00:00:00 EDT 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 23 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments
journal, August 2012
- Fan, C.; Cheng, S.; Sinha, S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 37
A Multiprotein Bicarbonate Dehydration Complex Essential to Carboxysome Function in Cyanobacteria
journal, November 2007
- Cot, S. S. -W.; So, A. K. -C.; Espie, G. S.
- Journal of Bacteriology, Vol. 190, Issue 3
Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans
journal, January 2013
- Petit, Elsa; LaTouf, W. Greg; Coppi, Maddalena V.
- PLoS ONE, Vol. 8, Issue 1
Isolation and Characterization of High CO 2 -Requiring-Mutants of the Cyanobacterium Synechococcus PCC7942 : Two Phenotypes that Accumulate Inorganic Carbon but Are Apparently Unable to Generate CO
journal, October 1989
- Price, G. D.; Badger, M. R.
- Plant Physiology, Vol. 91, Issue 2
Whole-Genome Transcription Profiling Reveals Genes Up-Regulated by Growth on Fucose in the Human Gut Bacterium "Roseburia inulinivorans"
journal, June 2006
- Scott, K. P.; Martin, J. C.; Campbell, G.
- Journal of Bacteriology, Vol. 188, Issue 12
Microcompartments for B12-Dependent 1,2-Propanediol Degradation Provide Protection from DNA and Cellular Damage by a Reactive Metabolic Intermediate
journal, February 2008
- Sampson, E. M.; Bobik, T. A.
- Journal of Bacteriology, Vol. 190, Issue 8, p. 2966-2971
The Propanediol Utilization (pdu) Operon ofSalmonella enterica Serovar Typhimurium LT2 Includes Genes Necessary for Formation of Polyhedral Organelles Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation
†
journal, January 1999
- Bobik, Thomas A.; Havemann, Gregory D.; Busch, Robert J.
- Journal of Bacteriology, Vol. 181, Issue 19
The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features
journal, January 2008
- Seedorf, H.; Fricke, W. F.; Veith, B.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 6
Genetic Analysis of the Protein Shell of the Microcompartments Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation by Salmonella
journal, January 2011
- Cheng, S.; Sinha, S.; Fan, C.
- Journal of Bacteriology, Vol. 193, Issue 6
Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins: Pentameric Structure of a Shell Protein from a Grp Microcompartment
journal, April 2013
- Wheatley, Nicole M.; Gidaniyan, Soheil D.; Liu, Yuxi
- Protein Science, Vol. 22, Issue 5
Functions, Compositions, and Evolution of the Two Types of Carboxysomes: Polyhedral Microcompartments That Facilitate CO2 Fixation in Cyanobacteria and Some Proteobacteria
journal, September 2013
- Rae, B. D.; Long, B. M.; Badger, M. R.
- Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
Short N-terminal sequences package proteins into bacterial microcompartments
journal, March 2010
- Fan, C.; Cheng, S.; Liu, Y.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 16
Procedure for Identifying Nonsense Mutations
journal, January 1968
- Berkowitz, David; Hushon, Judith M.; Whitfield, Harvey J.
- Journal of Bacteriology, Vol. 96, Issue 1
Engineering Bacterial Microcompartment Shells: Chimeric Shell Proteins and Chimeric Carboxysome Shells
journal, July 2014
- Cai, Fei; Sutter, Markus; Bernstein, Susan L.
- ACS Synthetic Biology, Vol. 4, Issue 4
Crystal structure of the EutL shell protein of the ethanolamine ammonia lyase microcompartment
journal, May 2009
- Sagermann, M.; Ohtaki, A.; Nikolakakis, K.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 22
The PduM Protein Is a Structural Component of the Microcompartments Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation by Salmonella enterica
journal, February 2012
- Sinha, S.; Cheng, S.; Fan, C.
- Journal of Bacteriology, Vol. 194, Issue 8
Atomic-Level Models of the Bacterial Carboxysome Shell
journal, February 2008
- Tanaka, S.; Kerfeld, C. A.; Sawaya, M. R.
- Science, Vol. 319, Issue 5866
The Shells of BMC-Type Microcompartment Organelles in Bacteria
journal, January 2013
- Yeates, Todd O.; Jorda, Julien; Bobik, Thomas A.
- Journal of Molecular Microbiology and Biotechnology, Vol. 23, Issue 4-5
The Alternative Electron Acceptor Tetrathionate Supports B12-Dependent Anaerobic Growth of Salmonella enterica Serovar Typhimurium on Ethanolamine or 1,2-Propanediol
journal, April 2001
- Price-Carter, M.; Tingey, J.; Bobik, T. A.
- Journal of Bacteriology, Vol. 183, Issue 8
PduA Is a Shell Protein of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2
journal, March 2002
- Havemann, G. D.; Sampson, E. M.; Bobik, T. A.
- Journal of Bacteriology, Vol. 184, Issue 5
In-gel digestion for mass spectrometric characterization of proteins and proteomes
journal, December 2006
- Shevchenko, Andrej; Tomas, Henrik; Havli, Jan
- Nature Protocols, Vol. 1, Issue 6
Conserving a Volatile Metabolite: a Role for Carboxysome-Like Organelles in Salmonella enterica
journal, April 2006
- Penrod, J. T.; Roth, J. R.
- Journal of Bacteriology, Vol. 188, Issue 8
Elucidating Essential Role of Conserved Carboxysomal Protein CcmN Reveals Common Feature of Bacterial Microcompartment Assembly
journal, March 2012
- Kinney, James N.; Salmeen, Annette; Cai, Fei
- Journal of Biological Chemistry, Vol. 287, Issue 21
Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme
journal, November 2012
- Craciun, S.; Balskus, E. P.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 52
Structural Insight into the Mechanisms of Transport across the Salmonella enterica Pdu Microcompartment Shell
journal, September 2010
- Crowley, Christopher S.; Cascio, Duilio; Sawaya, Michael R.
- Journal of Biological Chemistry, Vol. 285, Issue 48
Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway
journal, November 2013
- Cameron, Jeffrey C.; Wilson, Steven C.; Bernstein, Susan L.
- Cell, Vol. 155, Issue 5
Selective molecular transport through the protein shell of a bacterial microcompartment organelle
journal, February 2015
- Chowdhury, Chiranjit; Chun, Sunny; Pang, Allan
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 10
Construction and Characterization of a Highly Regulable Expression Vector, pLAC11, and Its Multipurpose Derivatives, pLAC22 and pLAC33
journal, September 2000
- Warren, James W.; Walker, Jennifer R.; Roth, John R.
- Plasmid, Vol. 44, Issue 2
Operon structure and cotranslational subunit association direct protein assembly in bacteria
journal, September 2015
- Shieh, Y. -W.; Minguez, P.; Bork, P.
- Science, Vol. 350, Issue 6261
A method for detection of phage mutants with altered transducing ability
journal, December 1971
- Schmieger, H.
- Molecular and General Genetics MGG, Vol. 110, Issue 4
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
Mapping nonselectable genes of Escherichia coli by using transposon Tn10: location of a gene affecting pyruvate oxidase.
journal, January 1982
- Chang, Y. Y.; Cronan, J. E.
- Journal of Bacteriology, Vol. 151, Issue 3
Substrate channels revealed in the trimeric Lactobacillus reuteri bacterial microcompartment shell protein PduB
journal, November 2012
- Pang, Allan; Liang, Mingzhi; Prentice, Michael B.
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 12
Structure of PduT, a trimeric bacterial microcompartment protein with a 4Fe–4S cluster-binding site
journal, January 2011
- Pang, Allan; Warren, Martin J.; Pickersgill, Richard W.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 2
Bacterial microcompartments: their properties and paradoxes
journal, November 2008
- Cheng, Shouqiang; Liu, Yu; Crowley, Christopher S.
- BioEssays, Vol. 30, Issue 11-12
Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria: Bacterial Microcompartments
journal, January 2013
- Jorda, Julien; Lopez, David; Wheatley, Nicole M.
- Protein Science, Vol. 22, Issue 2
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment
journal, April 2013
- Cai, Fei; Sutter, Markus; Cameron, Jeffrey C.
- Journal of Biological Chemistry, Vol. 288, Issue 22
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
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
journal, May 2000
- Datsenko, K. A.; Wanner, B. L.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
Synthesis of Empty Bacterial Microcompartments, Directed Organelle Protein Incorporation, and Evidence of Filament-Associated Organelle Movement
journal, April 2010
- Parsons, Joshua B.; Frank, Stefanie; Bhella, David
- Molecular Cell, Vol. 38, Issue 2
Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways: Bacterial microcompartments
journal, August 2015
- Bobik, Thomas A.; Lehman, Brent P.; Yeates, Todd O.
- Molecular Microbiology, Vol. 98, Issue 2
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
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
Protein Structures Forming the Shell of Primitive Bacterial Organelles
journal, August 2005
- Kerfeld, C. A.
- Science, Vol. 309, Issue 5736
Characterization of a Planctomycetal Organelle: a Novel Bacterial Microcompartment for the Aerobic Degradation of Plant Saccharides
journal, January 2014
- Erbilgin, Onur; McDonald, Kent L.; Kerfeld, Cheryl A.
- Applied and Environmental Microbiology, Vol. 80, Issue 7
Protein Content of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2
journal, August 2003
- Havemann, G. D.; Bobik, T. A.
- Journal of Bacteriology, Vol. 185, Issue 17
Structure of a trimeric bacterial microcompartment shell protein, EtuB, associated with ethanol utilization in Clostridium kluyveri
journal, September 2009
- Heldt, Dana; Frank, Stefanie; Seyedarabi, Arefeh
- Biochemical Journal, Vol. 423, Issue 2
Works referencing / citing this record:
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
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
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
The N Terminus of the PduB Protein Binds the Protein Shell of the Pdu Microcompartment to Its Enzymatic Core
journal, January 2017
- Lehman, Brent P.; Chowdhury, Chiranjit; Bobik, Thomas A.
- Journal of Bacteriology, Vol. 199, Issue 8
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
Broad-scale redistribution of mRNA abundance and transcriptional machinery in response to growth rate in Salmonella enterica serovar Typhimurium
journal, October 2017
- Cameron, Andrew D. S.; Dillon, Shane C.; Kröger, Carsten
- Microbial Genomics, Vol. 3, Issue 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
Successive Paradigm Shifts in the Bacterial Cell Cycle and Related Subjects
journal, March 2019
- Norris, Vic
- Life, Vol. 9, Issue 1