Comparative differential cuproproteomes of Rhodobacter capsulatus reveal novel copper homeostasis related proteins
Abstract
Abstract Copper (Cu) is an essential, but toxic, micronutrient for living organisms and cells have developed sophisticated response mechanisms towards both the lack and the excess of Cu in their environments. In this study, we achieved a global view of Cu-responsive changes in the prokaryotic model organism Rhodobacter capsulatus using label-free quantitative differential proteomics. Semi-aerobically grown cells under heterotrophic conditions in minimal medium (∼0.3 μM Cu) were compared with cells supplemented with either 5 μM Cu or with 5 mM of the Cu-chelator bathocuproine sulfonate. Mass spectrometry based bottom-up proteomics of unfractionated cell lysates identified 2430 of the 3632 putative proteins encoded by the genome, producing a robust proteome dataset for R. capsulatus. Use of biological and technical replicates for each growth condition yielded high reproducibility and reliable quantification for 1926 of the identified proteins. Comparison of cells grown under Cu-excess or Cu-depleted conditions to those grown under minimal Cu-sufficient conditions revealed that 75 proteins exhibited statistically significant (p < 0.05) abundance changes, ranging from 2- to 300-fold. A subset of the highly Cu-responsive proteins was orthogonally probed using molecular genetics, validating that several of them were indeed involved in cellular Cu homeostasis.
- Authors:
-
- Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA. Tel: +1 215 898 4394
- Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA. Tel: +1 215 898 4394, Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA
- Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA. Tel: +1 215 898 4394, Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs University of Freiburg, 79104 Freiburg, Germany
- Biology Department, Brookhaven National Laboratory, Upton, NY 11973, USA
- Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
- Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs University of Freiburg, 79104 Freiburg, Germany
- Publication Date:
- Research Org.:
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); German Research Foundation (DGK)
- OSTI Identifier:
- 1770458
- Alternate Identifier(s):
- OSTI ID: 1603716; OSTI ID: 1649987
- Report Number(s):
- BNL-216251-2020-JAAM
Journal ID: ISSN 1756-5901
- Grant/Contract Number:
- Quantitative Plant Science Initiative; DOE DE-FG02-91ER20052; SC0012704; FG02-91ER20052; GM 38237; GRK2202-235777276; IRTG1478; GM 110174
- Resource Type:
- Published Article
- Journal Name:
- Metallomics
- Additional Journal Information:
- Journal Name: Metallomics Journal Volume: 12 Journal Issue: 4; Journal ID: ISSN 1756-5901
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Rhodobacter capsulatus proteome; differential cuproproteomics; copper homeostasis; copper-responsive proteins; uncharacterized proteins
Citation Formats
Selamoglu, Nur, Önder, Özlem, Öztürk, Yavuz, Khalfaoui-Hassani, Bahia, Blaby-Haas, Crysten E., Garcia, Benjamin A., Koch, Hans-Georg, and Daldal, Fevzi. Comparative differential cuproproteomes of Rhodobacter capsulatus reveal novel copper homeostasis related proteins. United Kingdom: N. p., 2020.
Web. doi:10.1039/c9mt00314b.
Selamoglu, Nur, Önder, Özlem, Öztürk, Yavuz, Khalfaoui-Hassani, Bahia, Blaby-Haas, Crysten E., Garcia, Benjamin A., Koch, Hans-Georg, & Daldal, Fevzi. Comparative differential cuproproteomes of Rhodobacter capsulatus reveal novel copper homeostasis related proteins. United Kingdom. https://doi.org/10.1039/c9mt00314b
Selamoglu, Nur, Önder, Özlem, Öztürk, Yavuz, Khalfaoui-Hassani, Bahia, Blaby-Haas, Crysten E., Garcia, Benjamin A., Koch, Hans-Georg, and Daldal, Fevzi. Mon .
"Comparative differential cuproproteomes of Rhodobacter capsulatus reveal novel copper homeostasis related proteins". United Kingdom. https://doi.org/10.1039/c9mt00314b.
@article{osti_1770458,
title = {Comparative differential cuproproteomes of Rhodobacter capsulatus reveal novel copper homeostasis related proteins},
author = {Selamoglu, Nur and Önder, Özlem and Öztürk, Yavuz and Khalfaoui-Hassani, Bahia and Blaby-Haas, Crysten E. and Garcia, Benjamin A. and Koch, Hans-Georg and Daldal, Fevzi},
abstractNote = {Abstract Copper (Cu) is an essential, but toxic, micronutrient for living organisms and cells have developed sophisticated response mechanisms towards both the lack and the excess of Cu in their environments. In this study, we achieved a global view of Cu-responsive changes in the prokaryotic model organism Rhodobacter capsulatus using label-free quantitative differential proteomics. Semi-aerobically grown cells under heterotrophic conditions in minimal medium (∼0.3 μM Cu) were compared with cells supplemented with either 5 μM Cu or with 5 mM of the Cu-chelator bathocuproine sulfonate. Mass spectrometry based bottom-up proteomics of unfractionated cell lysates identified 2430 of the 3632 putative proteins encoded by the genome, producing a robust proteome dataset for R. capsulatus. Use of biological and technical replicates for each growth condition yielded high reproducibility and reliable quantification for 1926 of the identified proteins. Comparison of cells grown under Cu-excess or Cu-depleted conditions to those grown under minimal Cu-sufficient conditions revealed that 75 proteins exhibited statistically significant (p < 0.05) abundance changes, ranging from 2- to 300-fold. A subset of the highly Cu-responsive proteins was orthogonally probed using molecular genetics, validating that several of them were indeed involved in cellular Cu homeostasis.},
doi = {10.1039/c9mt00314b},
journal = {Metallomics},
number = 4,
volume = 12,
place = {United Kingdom},
year = {Mon Mar 09 00:00:00 EDT 2020},
month = {Mon Mar 09 00:00:00 EDT 2020}
}
https://doi.org/10.1039/c9mt00314b
Web of Science
Works referenced in this record:
Periplasmic proteins encoded by VCA0261–0260 and VC2216 genes together with copA and cueR products are required for copper tolerance but not for virulence in Vibrio cholerae
journal, August 2012
- Marrero, Karen; Sánchez, Aniel; González, Luis Javier
- Microbiology, Vol. 158, Issue 8
The cbb 3 -type cytochrome oxidase assembly factor CcoG is a widely distributed cupric reductase
journal, September 2019
- Marckmann, Dorian; Trasnea, Petru-Iulian; Schimpf, Johannes
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 42
Absence of Thiol-Disulfide Oxidoreductase DsbA Impairs cbb3-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus
journal, December 2017
- Onder, Ozlem; Verissimo, Andreia F.; Khalfaoui-Hassani, Bahia
- Frontiers in Microbiology, Vol. 8
A Requirement for Sodium in the Growth of Rhodopseudomonas spheroides
journal, June 1960
- Sistrom, W. R.
- Journal of General Microbiology, Vol. 22, Issue 3
The multicopper oxidase CutO confers copper tolerance to Rhodobacter capsulatus
journal, March 2006
- Wiethaus, Jessica; Wildner, Günter F.; Masepohl, Bernd
- FEMS Microbiology Letters, Vol. 256, Issue 1
Metal homeostasis and resistance in bacteria
journal, March 2017
- Chandrangsu, Pete; Rensing, Christopher; Helmann, John D.
- Nature Reviews Microbiology, Vol. 15, Issue 6
Mechanisms of copper homeostasis in bacteria
journal, January 2013
- Argüello, José M.; Raimunda, Daniel; Padilla-Benavides, Teresita
- Frontiers in Cellular and Infection Microbiology, Vol. 3
The ScoI homologue SenC is a copper binding protein that interacts directly with the cbb3-type cytochrome oxidase in Rhodobacter capsulatus
journal, November 2012
- Lohmeyer, Eva; Schröder, Sebastian; Pawlik, Grzegorz
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 11
Copper-responsive gene regulation in bacteria
journal, August 2012
- Rademacher, C.; Masepohl, B.
- Microbiology, Vol. 158, Issue Pt_10
Structural Basis of Biological N2O Generation by Bacterial Nitric Oxide Reductase
journal, November 2010
- Hino, T.; Matsumoto, Y.; Nagano, S.
- Science, Vol. 330, Issue 6011
Copper Homeostasis in Escherichia coli and Other Enterobacteriaceae
journal, April 2007
- Rensing, Christopher; Franke, Sylvia
- EcoSal Plus, Vol. 2, Issue 2
Structure and Function of Bacillus subtilis YphP, a Prokaryotic Disulfide Isomerase with a CXC Catalytic Motif ,
journal, September 2009
- Derewenda, Urszula; Boczek, Tomasz; Gorres, Kelly L.
- Biochemistry, Vol. 48, Issue 36
Coproporphyrin III excretion identifies the anaerobic coproporphyrinogen III oxidase HemN as a copper target in the Cu + -ATPase mutant copA − of Rubrivivax gelatinosus: Excess copper targets HemN in the tetrapyrrole biosynthesis pathway
journal, March 2013
- Azzouzi, Asma; Steunou, Anne-Soisig; Durand, Anne
- Molecular Microbiology, Vol. 88, Issue 2
Isolation and Characterization of Rhodobacter capsulatus Mutants Affected in Cytochromecbb
3 Oxidase Activity
journal, January 1998
- Koch, Hans-Georg; Hwang, Olivia; Daldal, Fevzi
- Journal of Bacteriology, Vol. 180, Issue 4
Cytochrome c biogenesis System I: An intricate process catalyzed by a maturase supercomplex?
journal, July 2014
- Verissimo, Andreia F.; Daldal, Fevzi
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria
journal, October 1988
- Keen, N. T.; Tamaki, S.; Kobayashi, D.
- Gene, Vol. 70, Issue 1
Development and dynamics of the photosynthetic apparatus in purple phototrophic bacteria
journal, March 2016
- Niederman, Robert A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 3
A Copper Relay System Involving Two Periplasmic Chaperones Drives cbb 3 -Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus
journal, April 2018
- Trasnea, Petru-Iulian; Andrei, Andreea; Marckmann, Dorian
- ACS Chemical Biology, Vol. 13, Issue 5
Bacterial copper storage proteins
journal, February 2018
- Dennison, Christopher; David, Sholto; Lee, Jaeick
- Journal of Biological Chemistry, Vol. 293, Issue 13
Biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus
journal, June 2012
- Ekici, Seda; Pawlik, Grzegorz; Lohmeyer, Eva
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6
Escherichia coli mechanisms of copper homeostasis in a changing environment
journal, June 2003
- Rensing, Christopher; Grass, Gregor
- FEMS Microbiology Reviews, Vol. 27, Issue 2-3
The copper-deprivation stimulon of Corynebacterium glutamicum comprises proteins for biogenesis of the actinobacterial cytochrome bc 1 – aa 3 supercomplex
journal, August 2018
- Morosov, Xenia; Davoudi, Cedric-Farhad; Baumgart, Meike
- Journal of Biological Chemistry, Vol. 293, Issue 40
Gene co-expression network analysis in Rhodobacter capsulatus and application to comparative expression analysis of Rhodobacter sphaeroides
journal, January 2014
- Peña-Castillo, Lourdes; Mercer, Ryan G.; Gurinovich, Anastasia
- BMC Genomics, Vol. 15, Issue 1
Cytochrome c2 is essential for electron transfer to nitrous oxide reductase from physiological substrates in Rhodobacter capsulatus and can act as an electron donor to the reductase in vitro. Correlation with photoinhibition studies
journal, August 1991
- Richardson, David J.; Bell, Louise C.; McEWAN, Alastair G.
- European Journal of Biochemistry, Vol. 199, Issue 3
Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans Are Specialized in the Maximal Viable Response to Heavy Metals
journal, August 2007
- Monchy, S.; Benotmane, M. A.; Janssen, P.
- Journal of Bacteriology, Vol. 189, Issue 20
Intracytoplasmic Copper Homeostasis Controls Cytochrome c Oxidase Production
journal, January 2014
- Ekici, Seda; Turkarslan, Serdar; Pawlik, Grzegorz
- mBio, Vol. 5, Issue 1
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification
journal, November 2008
- Cox, Jürgen; Mann, Matthias
- Nature Biotechnology, Vol. 26, Issue 12
Quorum-sensing regulation of a capsular polysaccharide receptor for the Rhodobacter capsulatus gene transfer agent (RcGTA): R . capsulatus gene transfer agent receptor
journal, January 2013
- Brimacombe, Cedric A.; Stevens, Aaron; Jun, Daniel
- Molecular Microbiology, Vol. 87, Issue 4
c-Type Cytochrome Assembly Is a Key Target of Copper Toxicity within the Bacterial Periplasm
journal, September 2015
- Durand, Anne; Azzouzi, Asma; Bourbon, Marie-Line
- mBio, Vol. 6, Issue 5
Recent developments in copper and zinc homeostasis in bacterial pathogens
journal, April 2014
- Braymer, Joseph J.; Giedroc, David P.
- Current Opinion in Chemical Biology, Vol. 19
Bradyrhizobium japonicumFixK2, a Crucial Distributor in the FixLJ-Dependent Regulatory Cascade for Control of Genes Inducible by Low Oxygen Levels
journal, January 1998
- Nellen-Anthamatten, D.; Rossi, P.; Preisig, O.
- Journal of Bacteriology, Vol. 180, Issue 19
Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases
journal, February 2018
- Khalfaoui-Hassani, Bahia; Wu, Hongjiang; Blaby-Haas, Crysten E.
- mBio, Vol. 9, Issue 1
Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34
journal, June 2006
- Monchy, Sébastien; Benotmane, Mohammed A.; Wattiez, Ruddy
- Microbiology, Vol. 152, Issue 6
Novel Transporter Required for Biogenesis of cbb3-Type Cytochrome c Oxidase in Rhodobacter capsulatus
journal, January 2012
- Ekici, Seda; Yang, Honghui; Koch, Hans-Georg
- mBio, Vol. 3, Issue 1
Proteome Profiling of the Rhodobacter capsulatus Molybdenum Response Reveals a Role of IscN in Nitrogen Fixation by Fe-Nitrogenase
journal, December 2015
- Hoffmann, Marie-Christine; Wagner, Eva; Langklotz, Sina
- Journal of Bacteriology, Vol. 198, Issue 4
In vitro insertional mutagenesis with a selectable DNA fragment
journal, September 1984
- Prentki, Pierre; Krisch, Henry M.
- Gene, Vol. 29, Issue 3
The Cu chaperone CopZ is required for Cu homeostasis in Rhodobacter capsulatus and influences cytochrome cbb 3 oxidase assembly : CopZ controls Cu homeostasis
journal, January 2019
- Utz, Marcel; Andrei, Andreea; Milanov, Martin
- Molecular Microbiology, Vol. 111, Issue 3
Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ
journal, June 2014
- Cox, Jürgen; Hein, Marco Y.; Luber, Christian A.
- Molecular & Cellular Proteomics, Vol. 13, Issue 9
The CopC Family: Structural and Bioinformatic Insights into a Diverse Group of Periplasmic Copper Binding Proteins
journal, April 2016
- Lawton, Thomas J.; Kenney, Grace E.; Hurley, Joseph D.
- Biochemistry, Vol. 55, Issue 15
The Distribution, Evolution, and Roles of Gene Transfer Agents in Prokaryotic Genetic Exchange
journal, September 2017
- Lang, Andrew S.; Westbye, Alexander B.; Beatty, J. Thomas
- Annual Review of Virology, Vol. 4, Issue 1
Andromeda: A Peptide Search Engine Integrated into the MaxQuant Environment
journal, April 2011
- Cox, Jürgen; Neuhauser, Nadin; Michalski, Annette
- Journal of Proteome Research, Vol. 10, Issue 4
Derived amino acid sequences of the nosZ gene (respiratory N2O reductase) from Alcaligenes eutrophus, Pseudomonas aeruginosa and Pseudomonas stutzeri reveal potential copper-binding residues. Implications for the CuA site of N2O reductase and cytochrome-c oxidase
journal, August 1992
- Zumft, Walter G.; Dreusch, Andreas; Lochelt, Sabine
- European Journal of Biochemistry, Vol. 208, Issue 1
Response of Gram-positive bacteria to copper stress
journal, September 2009
- Solioz, Marc; Abicht, Helge K.; Mermod, Mélanie
- JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 1
Copper tolerance and virulence in bacteria
journal, January 2015
- Ladomersky, Erik; Petris, Michael J.
- Metallomics, Vol. 7, Issue 6
Metallothionein diversity and distribution in the tree of life: a multifunctional protein
journal, January 2018
- Ziller, Antoine; Fraissinet-Tachet, Laurence
- Metallomics, Vol. 10, Issue 11
Copper homeostasis networks in the bacterium Pseudomonas aeruginosa
journal, July 2017
- Quintana, Julia; Novoa-Aponte, Lorena; Argüello, José M.
- Journal of Biological Chemistry, Vol. 292, Issue 38
Three-dimensional structure of the high-potential iron-sulfur protein isolated from the purple phototrophic bacterium Rhodocyclus tenuis determined and refined at 1.5 Å resolution
journal, November 1992
- Rayment, Ivan; Wesenberg, Gary; Meyer, Terry E.
- Journal of Molecular Biology, Vol. 228, Issue 2
Oxygen Activation Switch in the Copper Amine Oxidase of Escherichia coli
journal, August 2018
- Gaule, Thembaninkosi G.; Smith, Mark A.; Tych, Katarzyna M.
- Biochemistry, Vol. 57, Issue 36
How does nitrous oxide reductase interact with its electron donors?-A docking study
journal, April 2005
- Mattila, Kimmo; Haltia, Tuomas
- Proteins: Structure, Function, and Bioinformatics, Vol. 59, Issue 4
Copper Homeostasis in Salmonella Is Atypical and Copper-CueP Is a Major Periplasmic Metal Complex
journal, June 2010
- Osman, Deenah; Waldron, Kevin J.; Denton, Harriet
- Journal of Biological Chemistry, Vol. 285, Issue 33
Structural and Functional Proteomics of Intracytoplasmic Membrane Assembly in <b><i>Rhodobacter sphaeroides</i></b>
journal, January 2013
- Woronowicz, Kamil; Harrold, John W.; Kay, Joseph M.
- Journal of Molecular Microbiology and Biotechnology, Vol. 23, Issue 1-2
Zinc excess increases cellular demand for iron and decreases tolerance to copper in Escherichia coli
journal, October 2019
- Xu, Zeling; Wang, Pengchao; Wang, Haibo
- Journal of Biological Chemistry, Vol. 294, Issue 45
The SOS Response Master Regulator LexA Regulates the Gene Transfer Agent of Rhodobacter capsulatus and Represses Transcription of the Signal Transduction Protein CckA
journal, February 2016
- Kuchinski, Kevin S.; Brimacombe, Cedric A.; Westbye, Alexander B.
- Journal of Bacteriology, Vol. 198, Issue 7
Biochemical Physiology of a Respiration-Deficient Mutant of the Photosynthetic Bacterium Rhodopseudomonas capsulata
journal, April 1972
- Marrs, B.; Stahl, C. L.; Lien, S.
- Proceedings of the National Academy of Sciences, Vol. 69, Issue 4
Mobile Cytochrome c2 and Membrane-Anchored Cytochrome cy Are Both Efficient Electron Donors to the cbb3- and aa3-Type Cytochrome c Oxidases during Respiratory Growth of Rhodobacter sphaeroides
journal, March 2001
- Daldal, F.; Mandaci, S.; Winterstein, C.
- Journal of Bacteriology, Vol. 183, Issue 6
Transcriptional and Posttranscriptional Events Control Copper-Responsive Expression of a Rhodobacter capsulatus Multicopper Oxidase
journal, January 2012
- Rademacher, C.; Moser, R.; Lackmann, J. -W.
- Journal of Bacteriology, Vol. 194, Issue 8
The use of gene clusters to infer functional coupling
journal, March 1999
- Overbeek, R.; Fonstein, M.; D'Souza, M.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 6
Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata
journal, June 1979
- Yen, H. C.; Hu, N. T.; Marrs, B. L.
- Journal of Molecular Biology, Vol. 131, Issue 2
Copper Transport and Disease: What Can We Learn from Organoids?
journal, August 2019
- Pierson, Hannah; Yang, Haojun; Lutsenko, Svetlana
- Annual Review of Nutrition, Vol. 39, Issue 1
Biosynthesis of carotenoids derived from neurosporene in Rhodopseudomonas capsulata.
journal, March 1980
- Scolnik, P. A.; Walker, M. A.; Marrs, B. L.
- Journal of Biological Chemistry, Vol. 255, Issue 6
Bacterial Survival under Extreme UV Radiation: A Comparative Proteomics Study of Rhodobacter sp., Isolated from High Altitude Wetlands in Chile
journal, June 2017
- Pérez, Vilma; Hengst, Martha; Kurte, Lenka
- Frontiers in Microbiology, Vol. 8
Cytochrome c2 is not essential for photosynthetic growth of Rhodopseudomonas capsulata
journal, April 1986
- Daldal, F.; Cheng, S.; Applebaum, J.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 7
Copper Acquisition Is Mediated by YcnJ and Regulated by YcnK and CsoR in Bacillus subtilis
journal, January 2009
- Chillappagari, S.; Miethke, M.; Trip, H.
- Journal of Bacteriology, Vol. 191, Issue 7
Uncovering the Transmembrane Metal Binding Site of the Novel Bacterial Major Facilitator Superfamily-Type Copper Importer CcoA
journal, January 2016
- Khalfaoui-Hassani, Bahia; Verissimo, Andreia F.; Koch, Hans-Georg
- mBio, Vol. 7, Issue 1
Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria
journal, February 2019
- Zhang, Yang; Blaby-Haas, Crysten E.; Steimle, Stefan
- Scientific Reports, Vol. 9, Issue 1
Cellular copper management—a draft user's guide
journal, March 2010
- Bertini, Ivano; Cavallaro, Gabriele; McGreevy, Kathleen S.
- Coordination Chemistry Reviews, Vol. 254, Issue 5-6
Overproduction or Absence of the Periplasmic Protease DegP Severely Compromises Bacterial Growth in the Absence of the Dithiol: Disulfide Oxidoreductase DsbA
journal, January 2008
- Önder, Özlem; Turkarslan, Serdar; Sun, David
- Molecular & Cellular Proteomics, Vol. 7, Issue 5
Cooperation between two periplasmic copper chaperones is required for full activity of the cbb 3 -type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus : PccA-SenC interactions determine
journal, February 2016
- Trasnea, Petru-Iulian; Utz, Marcel; Khalfaoui-Hassani, Bahia
- Molecular Microbiology, Vol. 100, Issue 2
Riboregulators and the role of Hfq in photosynthetic bacteria
journal, February 2014
- Hess, Wolfgang R.; Berghoff, Bork A.; Wilde, Annegret
- RNA Biology, Vol. 11, Issue 5
Roles of the ccoGHIS gene products in the biogenesis of the cbb3-type cytochrome c oxidase
journal, March 2000
- Koch, Hans-Georg; Winterstein, Christine; Saribas, A. Sami
- Journal of Molecular Biology, Vol. 297, Issue 1