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The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene

Journal Article · · Molecular Microbiology
DOI:https://doi.org/10.1111/mmi.13423· OSTI ID:1328044
 [1];  [2];  [2];  [2];  [1]
  1. Iowa State Univ., Ames, IA (United States)
  2. Univ. of California, Los Angeles, CA (United States)
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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.
Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Organization:
National Center for Research Resources; National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1328044
Journal Information:
Molecular Microbiology, Journal Name: Molecular Microbiology Journal Issue: 5 Vol. 101; ISSN 0950-382X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
ENGLISH

References (50)

Bacterial microcompartments: their properties and paradoxes journal November 2008
Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria: Bacterial Microcompartments journal January 2013
Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins: Pentameric Structure of a Shell Protein from a Grp Microcompartment journal April 2013
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
Construction and Characterization of a Highly Regulable Expression Vector, pLAC11, and Its Multipurpose Derivatives, pLAC22 and pLAC33 journal September 2000
A method for detection of phage mutants with altered transducing ability journal December 1971
Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway journal November 2013
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport journal September 2009
Alanine Scanning Mutagenesis Identifies an Asparagine–Arginine–Lysine Triad Essential to Assembly of the Shell of the Pdu Microcompartment journal June 2014
Synthesis of Empty Bacterial Microcompartments, Directed Organelle Protein Incorporation, and Evidence of Filament-Associated Organelle Movement journal April 2010
Engineering Bacterial Microcompartment Shells: Chimeric Shell Proteins and Chimeric Carboxysome Shells journal July 2014
In-gel digestion for mass spectrometric characterization of proteins and proteomes journal December 2006
Structure of a trimeric bacterial microcompartment shell protein, EtuB, associated with ethanol utilization in Clostridium kluyveri journal September 2009
The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features journal January 2008
Crystal structure of the EutL shell protein of the ethanolamine ammonia lyase microcompartment journal May 2009
Short N-terminal sequences package proteins into bacterial microcompartments journal March 2010
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products journal May 2000
Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments journal August 2012
Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme journal November 2012
Selective molecular transport through the protein shell of a bacterial microcompartment organelle journal February 2015
Structural Insight into the Mechanisms of Transport across the Salmonella enterica Pdu Microcompartment Shell journal September 2010
Elucidating Essential Role of Conserved Carboxysomal Protein CcmN Reveals Common Feature of Bacterial Microcompartment Assembly journal March 2012
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment journal April 2013
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
Structure of PduT, a trimeric bacterial microcompartment protein with a 4Fe–4S cluster-binding site journal January 2011
Substrate channels revealed in the trimeric Lactobacillus reuteri bacterial microcompartment shell protein PduB journal November 2012
Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways: Bacterial microcompartments journal August 2015
Protein Structures Forming the Shell of Primitive Bacterial Organelles journal August 2005
Atomic-Level Models of the Bacterial Carboxysome Shell journal February 2008
Structure and Mechanisms of a Protein-Based Organelle in Escherichia coli journal December 2009
Operon structure and cotranslational subunit association direct protein assembly in bacteria journal September 2015
Characterization of a Planctomycetal Organelle: a Novel Bacterial Microcompartment for the Aerobic Degradation of Plant Saccharides journal January 2014
Whole-Genome Transcription Profiling Reveals Genes Up-Regulated by Growth on Fucose in the Human Gut Bacterium "Roseburia inulinivorans" journal June 2006
A Multiprotein Bicarbonate Dehydration Complex Essential to Carboxysome Function in Cyanobacteria journal November 2007
Genetic Analysis of the Protein Shell of the Microcompartments Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation by Salmonella journal January 2011
Microcompartments for B12-Dependent 1,2-Propanediol Degradation Provide Protection from DNA and Cellular Damage by a Reactive Metabolic Intermediate journal February 2008
The N-Terminal Region of the Medium Subunit (PduD) Packages Adenosylcobalamin-Dependent Diol Dehydratase (PduCDE) into the Pdu Microcompartment journal August 2011
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
Mapping nonselectable genes of Escherichia coli by using transposon Tn10: location of a gene affecting pyruvate oxidase. journal January 1982
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
The Alternative Electron Acceptor Tetrathionate Supports B12-Dependent Anaerobic Growth of Salmonella enterica Serovar Typhimurium on Ethanolamine or 1,2-Propanediol journal April 2001
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
Protein Content of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2 journal August 2003
Conserving a Volatile Metabolite: a Role for Carboxysome-Like Organelles in Salmonella enterica journal April 2006
Procedure for Identifying Nonsense Mutations journal January 1968
Diverse Bacterial Microcompartment Organelles journal September 2014
Functions, Compositions, and Evolution of the Two Types of Carboxysomes: Polyhedral Microcompartments That Facilitate CO2 Fixation in Cyanobacteria and Some Proteobacteria journal September 2013
Functional Genomics with a Comprehensive Library of Transposon Mutants for the Sulfate-Reducing Bacterium Desulfovibrio alaskensis G20 journal May 2014
The Shells of BMC-Type Microcompartment Organelles in Bacteria journal January 2013
Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans journal January 2013

Cited By (7)

Broad-scale redistribution of mRNA abundance and transcriptional machinery in response to growth rate in Salmonella enterica serovar Typhimurium journal October 2017
Engineering the Bacterial Microcompartment Domain for Molecular Scaffolding Applications journal July 2017
Successive Paradigm Shifts in the Bacterial Cell Cycle and Related Subjects journal March 2019
Building a toolbox of protein scaffolds for future immobilization of biocatalysts journal July 2018
Functional protein shells fabricated from the self-assembling protein sheets of prokaryotic organelles journal January 2020
Engineering the PduT shell protein to modify the permeability of the 1,2-propanediol microcompartment of Salmonella journal December 2019
The N Terminus of the PduB Protein Binds the Protein Shell of the Pdu Microcompartment to Its Enzymatic Core journal January 2017

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