A Copper Relay System Involving Two Periplasmic Chaperones Drives cbb3-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus

Trasnea, Petru-Iulian; Andrei, Andreea; Marckmann, Dorian; Utz, Marcel; Khalfaoui-Hassani, Bahia; Selamoglu, Nur; Daldal, Fevzi; Koch, Hans-Georg

doi:10.1021/acschembio.8b00293

A Copper Relay System Involving Two Periplasmic Chaperones Drives cbb₃-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus

Journal Article · Tue Apr 03 00:00:00 EDT 2018 · ACS Chemical Biology

DOI:https://doi.org/10.1021/acschembio.8b00293· OSTI ID:1546085

Trasnea, Petru-Iulian ^[1]; Andrei, Andreea ^[2]; Marckmann, Dorian ^[2]; Utz, Marcel ^[2]; Khalfaoui-Hassani, Bahia ^[3]; Selamoglu, Nur ^[3]; Daldal, Fevzi ^[3]; ^[2]

Univ. of Pennsylvania, Philadelphia, PA (United States); Univ. of Freiburg (Germany); None
Univ. of Freiburg (Germany)
Univ. of Pennsylvania, Philadelphia, PA (United States)

PccA and SenC are periplasmic copper chaperones required for the biogenesis of cbb₃-type cytochrome c oxidase (cbb₃-Cox) in Rhodobacter capsulatus at physiological Cu concentrations. However, both proteins are dispensable for cbb₃-Cox assembly when the external Cu concentration is high. PccA and SenC bind Cu using Met and His residues and Cys and His residues as ligands, respectively, and both proteins form a complex during cbb₃-Cox biogenesis. SenC also interacts directly with cbb₃-Cox, as shown by chemical cross-linking. Here we determined the periplasmic concentrations of both proteins in vivo and analyzed their Cu binding stoichiometries and their Cu(I) and Cu(II) binding affinity constants (KD) in vitro. Our data show that both proteins bind a single Cu atom with high affinity. In vitro Cu transfer assays demonstrate Cu transfer both from PccA to SenC and from SenC to PccA at similar levels. We conclude that PccA and SenC constitute a Cu relay system that facilitates Cu delivery to cbb₃-Cox.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Pennsylvania, Philadelphia, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: FG02-91ER20052

OSTI ID:: 1546085

Alternate ID(s):: OSTI ID: 1539519

Journal Information:: ACS Chemical Biology, Journal Name: ACS Chemical Biology Journal Issue: 5 Vol. 13; ISSN 1554-8929

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (45)

Roles of the ccoGHIS gene products in the biogenesis of the cbb3-type cytochrome c oxidase Koch, Hans-Georg; Winterstein, Christine; Saribas, A. Sami Journal of Molecular Biology, Vol. 297, Issue 1 https://doi.org/10.1006/jmbi.2000.3555	journal	March 2000
Cellular copper distribution: a mechanistic systems biology approach Banci, Lucia; Bertini, Ivano; Cantini, Francesca Cellular and Molecular Life Sciences, Vol. 67, Issue 15 https://doi.org/10.1007/s00018-010-0330-x	journal	March 2010
PrrC from Rhodobacter sphaeroides , a homologue of eukaryotic Sco proteins, is a copper-binding protein and may have a thiol-disulfide oxidoreductase activity McEwan, Alastair G.; Lewin, Allison; Davy, Sharon L. FEBS Letters, Vol. 518, Issue 1-3 https://doi.org/10.1016/S0014-5793(02)02532-2	journal	April 2002
Biogenesis of cytochrome c oxidase — in vitro approaches to study cofactor insertion into a bacterial subunit I Greiner, Peter; Hannappel, Achim; Werner, Carolin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 7-8 https://doi.org/10.1016/j.bbabio.2008.04.003	journal	July 2008
Differential affinity of BsSCO for Cu(II) and Cu(I) suggests a redox role in copper transfer to the CuA center of cytochrome c oxidase Hill, Bruce C.; Andrews, Diann Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6 https://doi.org/10.1016/j.bbabio.2011.09.006	journal	June 2012
Biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus Ekici, Seda; Pawlik, Grzegorz; Lohmeyer, Eva Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6 https://doi.org/10.1016/j.bbabio.2011.10.011	journal	June 2012
The roles of Rhodobacter sphaeroides copper chaperones PCuAC and Sco (PrrC) in the assembly of the copper centers of the aa3-type and the cbb3-type cytochrome c oxidases Thompson, Audie K.; Gray, Jimmy; Liu, Aimin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6 https://doi.org/10.1016/j.bbabio.2012.01.003	journal	June 2012
The ScoI homologue SenC is a copper binding protein that interacts directly with the cbb3-type cytochrome oxidase in Rhodobacter capsulatus Lohmeyer, Eva; Schröder, Sebastian; Pawlik, Grzegorz Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 11 https://doi.org/10.1016/j.bbabio.2012.06.621	journal	November 2012
Protein chaperones mediating copper insertion into the Cu A site of the aa 3 -type cytochrome c oxidase of Paracoccus denitrificans Dash, Banaja Priyadarshini; Alles, Melanie; Bundschuh, Freya Alena Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 2 https://doi.org/10.1016/j.bbabio.2014.11.001	journal	February 2015
Copper trafficking to the mitochondrion and assembly of copper metalloenzymes Cobine, Paul A.; Pierrel, Fabien; Winge, Dennis R. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 7 https://doi.org/10.1016/j.bbamcr.2006.03.002	journal	July 2006
PrrC, a Sco homologue from Rhodobacter sphaeroides , possesses thiol-disulfide oxidoreductase activity Badrick, Alison C.; Hamilton, Amanda J.; Bernhardt, Paul V. FEBS Letters, Vol. 581, Issue 24 https://doi.org/10.1016/j.febslet.2007.08.058	journal	September 2007
Copper chaperones. The concept of conformational control in the metabolism of copper Palumaa, Peep FEBS Letters, Vol. 587, Issue 13 https://doi.org/10.1016/j.febslet.2013.05.019	journal	May 2013
Coordination chemistry of copper proteins: How nature handles a toxic cargo for essential function Rubino, Jeffrey T.; Franz, Katherine J. Journal of Inorganic Biochemistry, Vol. 107, Issue 1 https://doi.org/10.1016/j.jinorgbio.2011.11.024	journal	February 2012
Multi-step Assembly Pathway of the cbb3-type Cytochrome c Oxidase Complex Kulajta, Carmen; Thumfart, Jörg Oliver; Haid, Sybille Journal of Molecular Biology, Vol. 355, Issue 5 https://doi.org/10.1016/j.jmb.2005.11.039	journal	February 2006
Rhodobacter capsulatus Contains a Novel cb-Type Cytochrome c Oxidase without a CuA Center Gray, Kevin A.; Grooms, Michael; Myllykallio, Hannu Biochemistry, Vol. 33, Issue 10 https://doi.org/10.1021/bi00176a047	journal	March 1994
Probing the Kinetics and Thermodynamics of Copper(II) Binding toBacillus subtilisSco, a Protein Involved in the Assembly of the Cu_ACenter of CytochromecOxidase Cawthorn, Thomas R.; Poulsen, Bradley E.; Davidson, David E. Biochemistry, Vol. 48, Issue 21 https://doi.org/10.1021/bi802288m	journal	June 2009
Copper Trafficking Mechanism of CXXC-Containing Domains: Insight from the pH-Dependence of Their Cu(I) Affinities Badarau, Adriana; Dennison, Christopher Journal of the American Chemical Society, Vol. 133, Issue 9 https://doi.org/10.1021/ja1091547	journal	March 2011
Affinity gradients drive copper to cellular destinations Banci, Lucia; Bertini, Ivano; Ciofi-Baffoni, Simone Nature, Vol. 465, Issue 7298 https://doi.org/10.1038/nature09018	journal	May 2010
Mechanism of CuA assembly Abriata, Luciano A.; Banci, Lucia; Bertini, Ivano Nature Chemical Biology, Vol. 4, Issue 10 https://doi.org/10.1038/nchembio.110	journal	August 2008
Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells Kulak, Nils A.; Pichler, Garwin; Paron, Igor Nature Methods, Vol. 11, Issue 3 https://doi.org/10.1038/nmeth.2834	journal	February 2014
Kinetic analysis of copper transfer from a chaperone to its target protein mediated by complex formation Kay, Kristine L.; Zhou, Liang; Tenori, Leonardo Chemical Communications, Vol. 53, Issue 8 https://doi.org/10.1039/C6CC08966F	journal	January 2017
The challenges of determining metal–protein affinities Xiao, Zhiguang; Wedd, Anthony G. Natural Product Reports, Vol. 27, Issue 5 https://doi.org/10.1039/b906690j	journal	January 2010
A copper(I) protein possibly involved in the assembly of CuA center of bacterial cytochrome c oxidase Banci, L.; Bertini, I.; Ciofi-Baffoni, S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 11 https://doi.org/10.1073/pnas.0406150102	journal	March 2005
A hint for the function of human Sco1 from different structures Banci, L.; Bertini, I.; Calderone, V. Proceedings of the National Academy of Sciences, Vol. 103, Issue 23 https://doi.org/10.1073/pnas.0601375103	journal	May 2006
Loop recognition and copper-mediated disulfide reduction underpin metal site assembly of Cu _A in human cytochrome oxidase Morgada, Marcos N.; Abriata, Luciano A.; Cefaro, Chiara Proceedings of the National Academy of Sciences, Vol. 112, Issue 38 https://doi.org/10.1073/pnas.1505056112	journal	September 2015
Disparate Pathways for the Biogenesis of Cytochrome Oxidases in Bradyrhizobium japonicum Bühler, Doris; Rossmann, Reinhild; Landolt, Sarah Journal of Biological Chemistry, Vol. 285, Issue 21 https://doi.org/10.1074/jbc.M109.085217	journal	March 2010
Copper Starvation-inducible Protein for Cytochrome Oxidase Biogenesis in Bradyrhizobium japonicum Serventi, Fabio; Youard, Zeb Andrew; Murset, Valérie Journal of Biological Chemistry, Vol. 287, Issue 46 https://doi.org/10.1074/jbc.M112.406173	journal	September 2012
How Periplasmic Thioredoxin TlpA Reduces Bacterial Copper Chaperone ScoI and Cytochrome Oxidase Subunit II (CoxB) Prior to Metallation* Abicht, Helge K.; Schärer, Martin A.; Quade, Nick Journal of Biological Chemistry, Vol. 289, Issue 47 https://doi.org/10.1074/jbc.M114.607127	journal	November 2014
Copper homeostasis networks in the bacterium Pseudomonas aeruginosa Quintana, Julia; Novoa-Aponte, Lorena; Argüello, José M. Journal of Biological Chemistry, Vol. 292, Issue 38 https://doi.org/10.1074/jbc.M117.804492	journal	July 2017
Specific Copper Transfer from the Cox17 Metallochaperone to Both Sco1 and Cox11 in the Assembly of Yeast Cytochrome c Oxidase Horng, Yih-Chern; Cobine, Paul A.; Maxfield, Andrew B. Journal of Biological Chemistry, Vol. 279, Issue 34 https://doi.org/10.1074/jbc.M404747200	journal	June 2004
The CyberCell Database (CCDB): a comprehensive, self-updating, relational database to coordinate and facilitate in silico modeling of Escherichia coli Sundararaj, S. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh108	journal	January 2004
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 Richardson, David J.; Bell, Louise C.; McEWAN, Alastair G. European Journal of Biochemistry, Vol. 199, Issue 3 https://doi.org/10.1111/j.1432-1033.1991.tb16170.x	journal	August 1991
Measurement of cell volume of phototrophic bacteria in pure cultures and natural samples: phase contrast, epifluorescence and particle sizing Gaju, NÃºria; Guerrero, Ricardo; PedrÃ³s-AliÃ³, Carlos FEMS Microbiology Letters, Vol. 62, Issue 5 https://doi.org/10.1111/j.1574-6968.1989.tb03383.x	journal	August 1989
The multicopper oxidase CutO confers copper tolerance to Rhodobacter capsulatus Wiethaus, Jessica; Wildner, GÃ¼nter F.; Masepohl, Bernd FEMS Microbiology Letters, Vol. 256, Issue 1 https://doi.org/10.1111/j.1574-6968.2005.00094.x	journal	March 2006
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 Trasnea, Petru-Iulian; Utz, Marcel; Khalfaoui-Hassani, Bahia Molecular Microbiology, Vol. 100, Issue 2 https://doi.org/10.1111/mmi.13321	journal	February 2016
The Structure of cbb3 Cytochrome Oxidase Provides Insights into Proton Pumping Buschmann, S.; Warkentin, E.; Xie, H. Science, Vol. 329, Issue 5989 https://doi.org/10.1126/science.1187303	journal	June 2010
Stability of the cbb3-Type Cytochrome Oxidase Requires Specific CcoQ-CcoP Interactions Peters, A.; Kulajta, C.; Pawlik, G. Journal of Bacteriology, Vol. 190, Issue 16 https://doi.org/10.1128/JB.00534-08	journal	June 2008
The Putative Assembly Factor CcoH Is Stably Associated with the cbb3-Type Cytochrome Oxidase Pawlik, G.; Kulajta, C.; Sachelaru, I. Journal of Bacteriology, Vol. 192, Issue 24 https://doi.org/10.1128/JB.00988-10	journal	October 2010
Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus. Buggy, J.; Bauer, C. E. Journal of bacteriology, Vol. 177, Issue 23 https://doi.org/10.1128/jb.177.23.6958-6965.1995	journal	January 1995
Novel Transporter Required for Biogenesis of cbb3-Type Cytochrome c Oxidase in Rhodobacter capsulatus Ekici, Seda; Yang, Honghui; Koch, Hans-Georg mBio, Vol. 3, Issue 1 https://doi.org/10.1128/mBio.00293-11	journal	January 2012
Intracytoplasmic Copper Homeostasis Controls Cytochrome c Oxidase Production Ekici, Seda; Turkarslan, Serdar; Pawlik, Grzegorz mBio, Vol. 5, Issue 1 https://doi.org/10.1128/mBio.01055-13	journal	January 2014
Roles of the Glutathione- and Thioredoxin-Dependent Reduction Systems in the Escherichia Coli and Saccharomyces Cerevisiae Responses to Oxidative Stress Carmel-Harel, Orna; Storz, Gisela Annual Review of Microbiology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.micro.54.1.439	journal	October 2000
Measurement of Cellular Copper in Rhodobacter capsulatus by Atomic Absorption Spectroscopy Trasnea, Petru-Iulian; Marckmann, Dorian; Utz, Marcel BIO-PROTOCOL, Vol. 6, Issue 19 https://doi.org/10.21769/BioProtoc.1948	journal	January 2016
Mechanisms of copper homeostasis in bacteria Argüello, José M.; Raimunda, Daniel; Padilla-Benavides, Teresita Frontiers in Cellular and Infection Microbiology, Vol. 3 https://doi.org/10.3389/fcimb.2013.00073	journal	January 2013
Absence of Thiol-Disulfide Oxidoreductase DsbA Impairs cbb3-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus Onder, Ozlem; Verissimo, Andreia F.; Khalfaoui-Hassani, Bahia Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02576	journal	December 2017

Cited By (2)

The regulation of oxidative phosphorylation pathway on Vibrio alginolyticus adhesion under adversities Huang, Li; Huang, Lixing; Zhao, Lingmin MicrobiologyOpen, Vol. 8, Issue 8 https://doi.org/10.1002/mbo3.805	journal	February 2019
Structural basis and mechanism for metallochaperone-assisted assembly of the CuA center in cytochrome oxidase Canonica, Fabia; Klose, Daniel; Ledermann, Raphael ETH Zurich https://doi.org/10.3929/ethz-b-000358191	text	January 2019

Similar Records

Cooperation between two periplasmic copper chaperones is required for full activity of the cbb₃-type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus

Journal Article · Sat Feb 27 23:00:00 EST 2016 · Molecular Microbiology · OSTI ID:1344916

The Cu chaperone CopZ is required for Cu homeostasis in Rhodobacter capsulatus and influences cytochrome cbb₃ oxidase assembly

Journal Article · Sun Dec 23 23:00:00 EST 2018 · Molecular Microbiology · OSTI ID:1597471

The CopA2-Type P_1B-Type ATPase CcoI Serves as Central Hub for cbb₃-Type Cytochrome Oxidase Biogenesis

Journal Article · Mon Sep 13 00:00:00 EDT 2021 · Frontiers in Microbiology · OSTI ID:1850003

Related Subjects

59 BASIC BIOLOGICAL SCIENCES