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Title: Bacterial microcompartments

Abstract

We report that bacterial microcompartments (BMCs) are self-assembling organelles that consist of an enzymatic core that is encapsulated by a selectively permeable protein shell. The potential to form BMCs is widespread and found across the kingdom Bacteria. BMCs have crucial roles in carbon dioxide fixation in autotrophs and the catabolism of organic substrates in heterotrophs. They contribute to the metabolic versatility of bacteria, providing a competitive advantage in specific environmental niches. Although BMCs were first visualized more than 60 years ago, it is mainly in the past decade that progress has been made in understanding their metabolic diversity and the structural basis of their assembly and function. This progress has not only heightened our understanding of their role in microbial metabolism but is also beginning to enable their use in a variety of applications in synthetic biology. In this work, we focus on recent insights into the structure, assembly, diversity and function of BMCs.

Authors:
 [1];  [2];  [3];  [4];  [1]
  1. Michigan State Univ., East Lansing, MI (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Michigan State Univ., East Lansing, MI (United States)
  3. Max Planck Institute for Terrestrial Microbiology, Marburg (Germany)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1485085
Grant/Contract Number:  
AC02-05CH11231; FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Nature Reviews Microbiology
Additional Journal Information:
Journal Volume: 16; Journal Issue: 5; Journal ID: ISSN 1740-1526
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Kerfeld, Cheryl A., Aussignargues, Clement, Zarzycki, Jan, Cai, Fei, and Sutter, Markus. Bacterial microcompartments. United States: N. p., 2018. Web. doi:10.1038/nrmicro.2018.10.
Kerfeld, Cheryl A., Aussignargues, Clement, Zarzycki, Jan, Cai, Fei, & Sutter, Markus. Bacterial microcompartments. United States. doi:10.1038/nrmicro.2018.10.
Kerfeld, Cheryl A., Aussignargues, Clement, Zarzycki, Jan, Cai, Fei, and Sutter, Markus. Mon . "Bacterial microcompartments". United States. doi:10.1038/nrmicro.2018.10. https://www.osti.gov/servlets/purl/1485085.
@article{osti_1485085,
title = {Bacterial microcompartments},
author = {Kerfeld, Cheryl A. and Aussignargues, Clement and Zarzycki, Jan and Cai, Fei and Sutter, Markus},
abstractNote = {We report that bacterial microcompartments (BMCs) are self-assembling organelles that consist of an enzymatic core that is encapsulated by a selectively permeable protein shell. The potential to form BMCs is widespread and found across the kingdom Bacteria. BMCs have crucial roles in carbon dioxide fixation in autotrophs and the catabolism of organic substrates in heterotrophs. They contribute to the metabolic versatility of bacteria, providing a competitive advantage in specific environmental niches. Although BMCs were first visualized more than 60 years ago, it is mainly in the past decade that progress has been made in understanding their metabolic diversity and the structural basis of their assembly and function. This progress has not only heightened our understanding of their role in microbial metabolism but is also beginning to enable their use in a variety of applications in synthetic biology. In this work, we focus on recent insights into the structure, assembly, diversity and function of BMCs.},
doi = {10.1038/nrmicro.2018.10},
journal = {Nature Reviews Microbiology},
number = 5,
volume = 16,
place = {United States},
year = {2018},
month = {3}
}

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Cited by: 37 works
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Figures / Tables:

Figure 1 Figure 1: Core biochemistry of carboxysomes and metabolosomes and superloci organization A) Schematic of the bacterial microcompartment (BMC) shell and encapsulated enzymes and associated flow of substrates/products. α-carboxysomes and β-carboxysomes both encapsulate carbonic anhydrase (CA) and Form 1 RuBisCO to fix CO2 as part of the Calvin-Benson-Bassham Cycle (CBB). Themore » shell prevents loss of CO2 to the cytoplasm. B) Metabolosomes have more diverse initial substrates compared to carboxysomes, but they typically share a common core biochemistry that is based on a signature enzyme, an aldehyde dehydrogenase (AldDH), an alcohol dehydrogenase (AlcDH) and a phosphotransacylase (PTAC). The signature enzyme generates the aldehyde which is then converted to a product alcohol by the AlcDH. This reaction uses CoA and NAD+ which are recycled in a separate reaction branch that uses AldDH and PTAC to produce a phosphorylated product (R-P). This product is then dephosphorylated by an acetyl kinase (AK) in a reaction that generates ATP. C) Schematic of a typical gene composition in a superlocus encoding a BMC. In addition to genes encoding shell and core proteins, BMC superloci encode proteins for supporting and ancillary functions, like transporters for the signature substrate. 3-PGA, 3-phosphoglycerate; RuBP, ribulose 1,5-bisphosphate;.« less

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Works referenced in this record:

Bacterial microcompartments and the modular construction of microbial metabolism
journal, January 2015


The Carboxysome Shell Is Permeable to Protons
journal, September 2010

  • Menon, B. B.; Heinhorst, S.; Shively, J. M.
  • Journal of Bacteriology, Vol. 192, Issue 22
  • DOI: 10.1128/JB.00903-10

Organization, Structure, and Assembly of α-Carboxysomes Determined by Electron Cryotomography of Intact Cells
journal, February 2010

  • Iancu, Cristina V.; Morris, Dylan M.; Dou, Zhicheng
  • Journal of Molecular Biology, Vol. 396, Issue 1
  • DOI: 10.1016/j.jmb.2009.11.019

Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes
journal, January 2017

  • Faulkner, Matthew; Rodriguez-Ramos, Jorge; Dykes, Gregory F.
  • Nanoscale, Vol. 9, Issue 30
  • DOI: 10.1039/C7NR02524F

Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans
journal, January 2013


Computational Design of Self-Assembling Protein Nanomaterials with Atomic Level Accuracy
journal, May 2012


Can the Cyanobacterial Carbon-Concentrating Mechanism Increase Photosynthesis in Crop Species? A Theoretical Analysis
journal, February 2014


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

The control region of the pdu/cob regulon in Salmonella typhimurium.
journal, September 1994


Bacterial microcompartment-directed polyphosphate kinase promotes stable polyphosphate accumulation in E. coli
journal, February 2017

  • Liang, Mingzhi; Frank, Stefanie; Lünsdorf, Heinrich
  • Biotechnology Journal, Vol. 12, Issue 3
  • DOI: 10.1002/biot.201600415

Plug-and-play for improving primary productivity
journal, December 2015


Pan-genome analysis of Clostridium botulinum reveals unique targets for drug development
journal, August 2017


A bioarchitectonic approach to the modular engineering of metabolism
journal, August 2017

  • Kerfeld, Cheryl A.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730
  • DOI: 10.1098/rstb.2016.0387

β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts
journal, June 2014

  • Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
  • The Plant Journal, Vol. 79, Issue 1
  • DOI: 10.1111/tpj.12536

Exploring Bacterial Organelle Interactomes: A Model of the Protein-Protein Interaction Network in the Pdu Microcompartment
journal, February 2015


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


Many-molecule encapsulation by an icosahedral shell
journal, May 2016

  • Perlmutter, Jason D.; Mohajerani, Farzaneh; Hagan, Michael F.
  • eLife, Vol. 5
  • DOI: 10.7554/eLife.14078

The PduL Phosphotransacylase Is Used To Recycle Coenzyme A within the Pdu Microcompartment
journal, May 2015

  • Liu, Yu; Jorda, Julien; Yeates, Todd O.
  • Journal of Bacteriology, Vol. 197, Issue 14
  • DOI: 10.1128/JB.00056-15

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
  • DOI: 10.1021/sb500226j

A SYNECHOCOCCUS PCC7942 Δ CCMM (CYANOPHYCEAE) MUTANT PSEUDOREVERTS TO AIR GROWTH WITHOUT REGAINING CARBOXYSOMES
journal, August 2006


Identification and characterization of the propanediol utilization protein PduP of Lactobacillus reuteri for 3-hydroxypropionic acid production from glycerol
journal, October 2010

  • Luo, Lian Hua; Seo, Jeong-Woo; Baek, Jin-Oh
  • Applied Microbiology and Biotechnology, Vol. 89, Issue 3
  • DOI: 10.1007/s00253-010-2887-6

Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome
journal, May 2007


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
  • DOI: 10.1073/pnas.0902324106

The robustness and innovability of protein folds
journal, June 2014


Sensing of Inorganic Carbon Limitation in Synechococcus PCC7942 Is Correlated with the Size of the Internal Inorganic Carbon Pool and Involves Oxygen
journal, November 2005

  • Woodger, Fiona J.; Badger, Murray R.; Price, G. Dean
  • Plant Physiology, Vol. 139, Issue 4
  • DOI: 10.1104/pp.105.069146

Spatially Ordered Dynamics of the Bacterial Carbon Fixation Machinery
journal, March 2010


Engineering nanoreactors using bacterial microcompartment architectures
journal, June 2018


A synthetic system for expression of components of a bacterial microcompartment
journal, September 2013


Enzyme Promiscuity: Engine of Evolutionary Innovation
journal, September 2014

  • Pandya, Chetanya; Farelli, Jeremiah D.; Dunaway-Mariano, Debra
  • Journal of Biological Chemistry, Vol. 289, Issue 44
  • DOI: 10.1074/jbc.R114.572990

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
  • DOI: 10.1073/pnas.1215689109

In Salmonella enterica, Ethanolamine Utilization Is Repressed by 1,2-Propanediol To Prevent Detrimental Mixing of Components of Two Different Bacterial Microcompartments
journal, May 2015

  • Sturms, Ryan; Streauslin, Nicholas A.; Cheng, Shouqiang
  • Journal of Bacteriology, Vol. 197, Issue 14
  • DOI: 10.1128/JB.00215-15

Isolation and Characterization of the Prochlorococcus Carboxysome Reveal the Presence of the Novel Shell Protein CsoS1D
journal, December 2011

  • Roberts, E. W.; Cai, F.; Kerfeld, C. A.
  • Journal of Bacteriology, Vol. 194, Issue 4
  • DOI: 10.1128/JB.06444-11

Modularity of a carbon-fixing protein organelle
journal, December 2011

  • Bonacci, W.; Teng, P. K.; Afonso, B.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 2
  • DOI: 10.1073/pnas.1108557109

Functional Organelles in Prokaryotes: Polyhedral Inclusions (Carboxysomes) of Thiobacillus neapolitanus
journal, November 1973


Heterologous expression of the Halothiobacillus neapolitanus carboxysomal gene cluster in Corynebacterium glutamicum
journal, September 2017


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
  • DOI: 10.1073/pnas.1423672112

Programmed Ribosomal Frameshifting Mediates Expression of the α-Carboxysome
journal, January 2016

  • Chaijarasphong, Thawatchai; Nichols, Robert J.; Kortright, Kaitlyn E.
  • Journal of Molecular Biology, Vol. 428, Issue 1
  • DOI: 10.1016/j.jmb.2015.11.017

The structure, kinetics and interactions of the β-carboxysomal β-carbonic anhydrase, CcaA
journal, December 2016

  • McGurn, Leah D.; Moazami-Goudarzi, Maryam; White, Sean A.
  • Biochemical Journal, Vol. 473, Issue 24
  • DOI: 10.1042/BCJ20160773

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

Evidence that a Metabolic Microcompartment Contains and Recycles Private Cofactor Pools
journal, April 2013

  • Huseby, D. L.; Roth, J. R.
  • Journal of Bacteriology, Vol. 195, Issue 12
  • DOI: 10.1128/JB.02179-12

Streamlined Construction of the Cyanobacterial CO 2 -Fixing Organelle via Protein Domain Fusions for Use in Plant Synthetic Biology
journal, August 2015

  • Gonzalez-Esquer, C. Raul; Shubitowski, Tyler B.; Kerfeld, Cheryl A.
  • The Plant Cell, Vol. 27, Issue 9
  • DOI: 10.1105/tpc.15.00329

Enterococcus faecalis Mutations Affecting Virulence in the Caenorhabditis elegans Model Host
journal, February 2007

  • Maadani, A.; Fox, K. A.; Mylonakis, E.
  • Infection and Immunity, Vol. 75, Issue 5
  • DOI: 10.1128/IAI.01372-06

Structure and Function of CutC Choline Lyase from Human Microbiota Bacterium Klebsiella pneumoniae
journal, July 2015

  • Kalnins, Gints; Kuka, Janis; Grinberga, Solveiga
  • Journal of Biological Chemistry, Vol. 290, Issue 35
  • DOI: 10.1074/jbc.M115.670471

Bacterial microcompartments as metabolic modules for plant synthetic biology
journal, June 2016

  • Gonzalez-Esquer, C. Raul; Newnham, Sarah E.; Kerfeld, Cheryl A.
  • The Plant Journal, Vol. 87, Issue 1
  • DOI: 10.1111/tpj.13166

The Structure of Isolated Synechococcus Strain WH8102 Carboxysomes as Revealed by Electron Cryotomography
journal, September 2007

  • Iancu, Cristina V.; Ding, H. Jane; Morris, Dylan M.
  • Journal of Molecular Biology, Vol. 372, Issue 3
  • DOI: 10.1016/j.jmb.2007.06.059

Insights from 20 years of bacterial genome sequencing
journal, February 2015

  • Land, Miriam; Hauser, Loren; Jun, Se-Ran
  • Functional & Integrative Genomics, Vol. 15, Issue 2
  • DOI: 10.1007/s10142-015-0433-4

1,2-Propanediol Dehydration in Roseburia inulinivorans : STRUCTURAL BASIS FOR SUBSTRATE AND ENANTIOMER SELECTIVITY
journal, June 2016

  • LaMattina, Joseph W.; Keul, Nicholas D.; Reitzer, Pierre
  • Journal of Biological Chemistry, Vol. 291, Issue 30
  • DOI: 10.1074/jbc.M116.721142

Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function.
journal, May 1993


Cyanobacterial-based approaches to improving photosynthesis in plants
journal, October 2012

  • Zarzycki, Jan; Axen, Seth D.; Kinney, James N.
  • Journal of Experimental Botany, Vol. 64, Issue 3
  • DOI: 10.1093/jxb/ers294

Structure and Mechanisms of a Protein-Based Organelle in Escherichia coli
journal, December 2009


Characterization of Choline Trimethylamine-Lyase Expands the Chemistry of Glycyl Radical Enzymes
journal, May 2014

  • Craciun, Smaranda; Marks, Jonathan A.; Balskus, Emily P.
  • ACS Chemical Biology, Vol. 9, Issue 7
  • DOI: 10.1021/cb500113p

Bioinformatic Characterization of Glycyl Radical Enzyme-Associated Bacterial Microcompartments
journal, September 2015

  • Zarzycki, Jan; Erbilgin, Onur; Kerfeld, Cheryl A.
  • Applied and Environmental Microbiology, Vol. 81, Issue 24
  • DOI: 10.1128/AEM.02587-15

In the light of directed evolution: Pathways of adaptive protein evolution
journal, June 2009

  • Bloom, J. D.; Arnold, F. H.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue Supplement_1
  • DOI: 10.1073/pnas.0901522106

Engineered Protein Nano-Compartments for Targeted Enzyme Localization
journal, March 2012


Engineering formation of multiple recombinant Eut protein nanocompartments in E. coli
journal, April 2016

  • Held, Mark; Kolb, Alexander; Perdue, Sarah
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep24359

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
  • DOI: 10.1107/S0907444910050201

Theoretical Study of the Initial Stages of Self-Assembly of a Carboxysome’s Facet
journal, March 2016


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

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
  • DOI: 10.1074/jbc.M113.456897

Characterization and Detection of a Widely Distributed Gene Cluster That Predicts Anaerobic Choline Utilization by Human Gut Bacteria
journal, April 2015

  • Martínez-del Campo, Ana; Bodea, Smaranda; Hamer, Hilary A.
  • mBio, Vol. 6, Issue 2
  • DOI: 10.1128/mBio.00042-15

The Structural Basis of Coenzyme A Recycling in a Bacterial Organelle
journal, March 2016


Crystal structures of β-carboxysome shell protein CcmP: ligand binding correlates with the closed or open central pore
journal, March 2017

  • Larsson, Anna M.; Hasse, Dirk; Valegård, Karin
  • Journal of Experimental Botany, Vol. 68, Issue 14
  • DOI: 10.1093/jxb/erx070

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

Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis
journal, April 2013

  • Koeth, Robert A.; Wang, Zeneng; Levison, Bruce S.
  • Nature Medicine, Vol. 19, Issue 5
  • DOI: 10.1038/nm.3145

Unique Thylakoid Membrane Architecture of a Unicellular N 2 -Fixing Cyanobacterium Revealed by Electron Tomography
journal, December 2010

  • Liberton, Michelle; Austin, Jotham R.; Berg, R. Howard
  • Plant Physiology, Vol. 155, Issue 4
  • DOI: 10.1104/pp.110.165332

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


Monitoring Cytosolic pH of Carboxysome-Deficient Cells of Synechocystis sp. PCC 6803 Using Fluorescence Analysis
journal, July 2005


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
  • DOI: 10.1128/AEM.03887-13

The Pentameric Vertex Proteins Are Necessary for the Icosahedral Carboxysome Shell to Function as a CO2 Leakage Barrier
journal, October 2009


Engineering bacterial microcompartments with heterologous enzyme cargos
journal, September 2016

  • Wagner, Hanna J.; Capitain, Charlotte C.; Richter, Karsten
  • Engineering in Life Sciences, Vol. 17, Issue 1
  • DOI: 10.1002/elsc.201600107

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


A systems-level model reveals that 1,2-Propanediol utilization microcompartments enhance pathway flux through intermediate sequestration
journal, May 2017

  • Jakobson, Christopher M.; Tullman-Ercek, Danielle; Slininger, Marilyn F.
  • PLOS Computational Biology, Vol. 13, Issue 5
  • DOI: 10.1371/journal.pcbi.1005525

Dietary trimethylamine N-oxide exacerbates impaired glucose tolerance in mice fed a high fat diet
journal, October 2014


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
  • DOI: 10.1073/pnas.1207516109

Purification and some properties of wild-type and N-terminal-truncated ethanolamine ammonia-lyase of Escherichia coli
journal, September 2009

  • Akita, K.; Hieda, N.; Baba, N.
  • Journal of Biochemistry, Vol. 147, Issue 1
  • DOI: 10.1093/jb/mvp145

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
  • DOI: 10.1128/JB.01283-07

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
  • DOI: 10.1128/JB.00785-16

A single regulatory gene integrates control of vitamin B12 synthesis and propanediol degradation.
journal, April 1992


Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ
journal, November 2015

  • Sutter, Markus; Roberts, Evan W.; Gonzalez, Raul C.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep16243

Identification of Listeria monocytogenes Genes Contributing to Intracellular Replication by Expression Profiling and Mutant Screening
journal, December 2005


Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics
journal, June 2015

  • Nobu, Masaru K.; Dodsworth, Jeremy A.; Murugapiran, Senthil K.
  • The ISME Journal, Vol. 10, Issue 2
  • DOI: 10.1038/ismej.2015.97

Halothiobacillus neapolitanus Carboxysomes Sequester Heterologous and Chimeric RubisCO Species
journal, October 2008


Carboxysomal carbonic anhydrases: Structure and role in microbial CO2 fixation
journal, February 2010

  • Cannon, Gordon C.; Heinhorst, Sabine; Kerfeld, Cheryl A.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 2
  • DOI: 10.1016/j.bbapap.2009.09.026

Mechanism of formation of chloropropanols present in protein hydrolysates
journal, October 1991

  • Collier, P. D.; Cromie, D. D. O.; Davies, A. P.
  • Journal of the American Oil Chemists' Society, Vol. 68, Issue 10
  • DOI: 10.1007/BF02662173

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
  • DOI: 10.1128/MMBR.00061-12

Functional Cyanobacterial β -Carboxysomes Have an Absolute Requirement for Both Long and Short Forms of the CcmM Protein
journal, March 2010

  • Long, Benedict M.; Tucker, Loraine; Badger, Murray R.
  • Plant Physiology, Vol. 153, Issue 1
  • DOI: 10.1104/pp.110.154948

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

The complete genome sequence of Clostridium indolis DSM 755T
journal, March 2014

  • Biddle, Amy S.; Leschine, Susan; Huntemann, Marcel
  • Standards in Genomic Sciences, Vol. 9, Issue 3
  • DOI: 10.4056/sigs.5281010

Bacterial Microcompartments
journal, October 2010


A rapid flow cytometry assay for the relative quantification of protein encapsulation into bacterial microcompartments
journal, January 2014


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
  • DOI: 10.1073/pnas.0913199107

Localization of Proteins to the 1,2-Propanediol Utilization Microcompartment by Non-native Signal Sequences Is Mediated by a Common Hydrophobic Motif
journal, August 2015

  • Jakobson, Christopher M.; Kim, Edward Y.; Slininger, Marilyn F.
  • Journal of Biological Chemistry, Vol. 290, Issue 40
  • DOI: 10.1074/jbc.M115.651919

Dumpster Diving in the Gut: Bacterial Microcompartments as Part of a Host-Associated Lifestyle
journal, May 2016


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

A faster Rubisco with potential to increase photosynthesis in crops
journal, September 2014

  • Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
  • Nature, Vol. 513, Issue 7519
  • DOI: 10.1038/nature13776

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


Assembly, function and evolution of cyanobacterial carboxysomes
journal, June 2016


Biochemical and Structural Insights into Bacterial Organelle Form and Biogenesis
journal, March 2008

  • Parsons, Joshua B.; Dinesh, Sriramulu D.; Deery, Evelyne
  • Journal of Biological Chemistry, Vol. 283, Issue 21
  • DOI: 10.1074/jbc.M709214200

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


Atomic-Level Models of the Bacterial Carboxysome Shell
journal, February 2008


Synthetic protein scaffolds provide modular control over metabolic flux
journal, August 2009

  • Dueber, John E.; Wu, Gabriel C.; Malmirchegini, G. Reza
  • Nature Biotechnology, Vol. 27, Issue 8, p. 753-759
  • DOI: 10.1038/nbt.1557

In Vitro Characterization and Concerted Function of Three Core Enzymes of a Glycyl Radical Enzyme - Associated Bacterial Microcompartment
journal, February 2017

  • Zarzycki, Jan; Sutter, Markus; Cortina, Niña Socorro
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep42757

Global regulation by CsrA in Salmonella typhimurium: S. typhimurium CsrA global regulation
journal, May 2003


A Dodecameric CcmK2 Structure Suggests β-Carboxysomal Shell Facets Have a Double-Layered Organization
journal, August 2012


De novo design of signal sequences to localize cargo to the 1,2-propanediol utilization microcompartment : Design of Signal Sequences
journal, April 2017

  • Jakobson, Christopher M.; Slininger Lee, Marilyn F.; Tullman-Ercek, Danielle
  • Protein Science, Vol. 26, Issue 5
  • DOI: 10.1002/pro.3144

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
  • DOI: 10.1074/jbc.M112.355305

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

Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota
journal, October 2011

  • Thiennimitr, P.; Winter, S. E.; Winter, M. G.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 42
  • DOI: 10.1073/pnas.1107857108

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


The N-Terminal Regions of β and γ Subunits Lower the Solubility of Adenosylcobalamin-Dependent Diol Dehydratase
journal, January 2005

  • Tobimatsu, Takamasa; Kawata, Masahiro; Toraya, Tetsuo
  • Bioscience, Biotechnology, and Biochemistry, Vol. 69, Issue 3
  • DOI: 10.1271/bbb.69.455

Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease
journal, April 2011

  • Wang, Zeneng; Klipfell, Elizabeth; Bennett, Brian J.
  • Nature, Vol. 472, Issue 7341
  • DOI: 10.1038/nature09922

Nanotechnology: A New Opportunity in Plant Sciences
journal, August 2016


Plasma Choline Metabolites and Colorectal Cancer Risk in the Women's Health Initiative Observational Study
journal, October 2014


Intestinal Microbiota Composition Modulates Choline Bioavailability from Diet and Accumulation of the Proatherogenic Metabolite Trimethylamine-N-Oxide
journal, March 2015

  • Romano, Kymberleigh A.; Vivas, Eugenio I.; Amador-Noguez, Daniel
  • mBio, Vol. 6, Issue 2
  • DOI: 10.1128/mBio.02481-14

Bacterial microcompartments moving into a synthetic biological world
journal, January 2013


Structural basis of the oxidative activation of the carboxysomal  -carbonic anhydrase, CcmM
journal, January 2010

  • Pena, K. L.; Castel, S. E.; de Araujo, C.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 6
  • DOI: 10.1073/pnas.0910866107

Genetic analysis around aminoalcohol dehydrogenase gene of Rhodococcus erythropolis MAK154: a putative GntR transcription factor in transcriptional regulation
journal, October 2010

  • Urano, Nobuyuki; Kataoka, Michihiko; Ishige, Takeru
  • Applied Microbiology and Biotechnology, Vol. 89, Issue 3
  • DOI: 10.1007/s00253-010-2924-5

Protein-based organelles in bacteria: carboxysomes and related microcompartments
journal, August 2008

  • Yeates, Todd O.; Kerfeld, Cheryl A.; Heinhorst, Sabine
  • Nature Reviews Microbiology, Vol. 6, Issue 9
  • DOI: 10.1038/nrmicro1913

Tuning the Catalytic Activity of Subcellular Nanoreactors
journal, July 2016

  • Jakobson, Christopher M.; Chen, Yiqun; Slininger, Marilyn F.
  • Journal of Molecular Biology, Vol. 428, Issue 15
  • DOI: 10.1016/j.jmb.2016.07.006

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
  • DOI: 10.1107/S0907444912039315

Carboxysomes: metabolic modules for CO2 fixation
journal, August 2017

  • Turmo, Aiko; Gonzalez-Esquer, C. Raul; Kerfeld, Cheryl A.
  • FEMS Microbiology Letters, Vol. 364, Issue 18
  • DOI: 10.1093/femsle/fnx176

The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species
journal, October 2012

  • Price, G. Dean; Pengelly, Jasper J. L.; Forster, Britta
  • Journal of Experimental Botany, Vol. 64, Issue 3
  • DOI: 10.1093/jxb/ers257

Characterisation of PduS, the pdu Metabolosome Corrin Reductase, and Evidence of Substructural Organisation within the Bacterial Microcompartment
journal, November 2010


Diverse Bacterial Microcompartment Organelles
journal, September 2014

  • Chowdhury, C.; Sinha, S.; Chun, S.
  • Microbiology and Molecular Biology Reviews, Vol. 78, Issue 3
  • DOI: 10.1128/MMBR.00009-14

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

Ethanolamine Utilization Contributes to Proliferation of Salmonella enterica Serovar Typhimurium in Food and in Nematodes
journal, October 2010

  • Srikumar, Shabarinath; Fuchs, Thilo M.
  • Applied and Environmental Microbiology, Vol. 77, Issue 1
  • DOI: 10.1128/AEM.01403-10

Structural Insight into the Clostridium difficile Ethanolamine Utilisation Microcompartment
journal, October 2012


Analysis of Carboxysomes from Synechococcus PCC7942 Reveals Multiple Rubisco Complexes with Carboxysomal Proteins CcmM and CcaA
journal, August 2007

  • Long, Benedict M.; Badger, Murray R.; Whitney, Spencer M.
  • Journal of Biological Chemistry, Vol. 282, Issue 40
  • DOI: 10.1074/jbc.M703896200

Isoform specificity of trimethylamine N-oxygenation by human flavin-containing monooxygenase (FMO) and P450 enzymes
journal, October 1998


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

Comparative analysis of carboxysome shell proteins
journal, January 2011

  • Kinney, James N.; Axen, Seth D.; Kerfeld, Cheryl A.
  • Photosynthesis Research, Vol. 109, Issue 1-3
  • DOI: 10.1007/s11120-011-9624-6

The PduQ Enzyme Is an Alcohol Dehydrogenase Used to Recycle NAD+ Internally within the Pdu Microcompartment of Salmonella enterica
journal, October 2012


The Bacterial Carbon-Fixing Organelle Is Formed by Shell Envelopment of Preassembled Cargo
journal, September 2013


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

Evidence for Improved Encapsulated Pathway Behavior in a Bacterial Microcompartment through Shell Protein Engineering
journal, June 2017

  • Slininger Lee, Marilyn F.; Jakobson, Christopher M.; Tullman-Ercek, Danielle
  • ACS Synthetic Biology, Vol. 6, Issue 10
  • DOI: 10.1021/acssynbio.7b00042

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

Crystal Structures of Ethanolamine Ammonia-lyase Complexed with Coenzyme B 12 Analogs and Substrates
journal, June 2010

  • Shibata, Naoki; Tamagaki, Hiroko; Hieda, Naoki
  • Journal of Biological Chemistry, Vol. 285, Issue 34
  • DOI: 10.1074/jbc.M110.125112

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
  • DOI: 10.1042/BJ20090780

    Works referencing / citing this record:

    Comparative Genomic Analysis Reveals Novel Microcompartment-Associated Metabolic Pathways in the Human Gut Microbiome
    journal, July 2019


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.