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

Trasnea, Petru -Iulian; Utz, Marcel; Khalfaoui-Hassani, Bahia; Lagies, Simon; Daldal, Fevzi; Koch, Hans -Georg

doi:10.1111/mmi.13321

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 · Sun Feb 28 00:00:00 EST 2016 · Molecular Microbiology

DOI:https://doi.org/10.1111/mmi.13321· OSTI ID:1344916

Trasnea, Petru -Iulian ^[1]; Utz, Marcel ^[2]; Khalfaoui-Hassani, Bahia ^[3]; Lagies, Simon ^[2]; Daldal, Fevzi ^[3]; Koch, Hans -Georg ^[2]

Institut fur Biochemie und Molekularbiologie, Freiburg (Germany); Albert-Ludwigs-Univ. Freiburg, Freiburg (Germany); DOE Office of Scientific and Technical Information (OSTI)
Institut fur Biochemie und Molekularbiologie, Freiburg (Germany)
Univ. of Pennsylvania, Philadelphia, PA (United States)

Copper (Cu) is an essential micronutrient that functions as a cofactor in several important enzymes, like respiratory heme-copper oxygen reductases. Yet, Cu is also toxic and therefore cells engage a highly coordinated Cu uptake and delivery system to prevent the accumulation of toxic Cu concentrations. In the current work we analyzed Cu delivery to the cbb₃-type cytochrome c oxidase (cbb₃-Cox) of Rhodobacter capsulatus. We identified the PCu_AC-like periplasmic chaperone PccA and analyzed its contribution to cbb₃-Cox assembly. Our data demonstrate that PccA is a Cu-binding protein with a preference for Cu(I), which is required for efficient cbb₃-Cox assembly, in particular at low Cu concentrations. By using in vivo and in vitro crosslinking we show that PccA forms a complex with the Sco1-homologue SenC. This complex is stabilized in the absence of the cbb₃-Cox specific assembly factors CcoGHIS. In cells lacking SenC, the cytoplasmic Cu content is significantly increased, but the simultaneous absence of PccA prevents this Cu accumulation. Lastly, these data demonstrate that the interplay between PccA and SenC is not only required for Cu delivery during cbb₃-Cox assembly, but that it also regulates Cu homeostasis in R. capsulatus.

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:: 1344916

Journal Information:: Molecular Microbiology, Journal Name: Molecular Microbiology Journal Issue: 2 Vol. 100; ISSN 0950-382X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

A novel membrane-associated c-type cytochrome, cyt cy, can mediate the photosynthetic growth of Rhodobacter capsulatus and Rhodobacter sphaeroides. Jenney, F. E.; Daldal, F. The EMBO Journal, Vol. 12, Issue 4 https://doi.org/10.1002/j.1460-2075.1993.tb05773.x	journal	April 1993
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
Genes for a second terminal oxidase in Bradyrhizobium japonicum Bott, Michael; Preisig, Oliver; Hennecke, Hauke Archives of Microbiology, Vol. 158, Issue 5 https://doi.org/10.1007/BF00245362	journal	October 1992
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
The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb 3 -type cytochrome oxidase Preisig, O.; Zufferey, Rachel; Hennecke, H. Archives of Microbiology, Vol. 165, Issue 5 https://doi.org/10.1007/s002030050330	journal	May 1996
The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function Raimunda, Daniel; González-Guerrero, Manuel; Leeber, Blaise W. BioMetals, Vol. 24, Issue 3 https://doi.org/10.1007/s10534-010-9404-3	journal	January 2011
Cytochrome c oxidase: exciting progress and remaining mysteries Brzezinski, Peter; Gennis, Robert B. Journal of Bioenergetics and Biomembranes, Vol. 40, Issue 5 https://doi.org/10.1007/s10863-008-9181-7	journal	October 2008
An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels Thomas, Paul E.; Ryan, Dene; Levin, Wayne Analytical Biochemistry, Vol. 75, Issue 1 https://doi.org/10.1016/0003-2697(76)90067-1	journal	September 1976
Site-directed mutagenesis of cytochrome c oxidase reveals two acidic residues involved in the binding of cytochrome c Witt, Heike; Zickermann, Volker; Ludwig, Bernd Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1230, Issue 1-2 https://doi.org/10.1016/0005-2728(95)00050-S	journal	June 1995
Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and φ80 transducing phages Brickman, Edith; Beckwith, Jon Journal of Molecular Biology, Vol. 96, Issue 2 https://doi.org/10.1016/0022-2836(75)90350-2	journal	August 1975
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 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
Biogenesis/assembly of respiratory enzyme complexes Hosler, Jonathan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6 https://doi.org/10.1016/j.bbabio.2012.04.014	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
The Human Cytochrome c Oxidase Assembly Factors SCO1 and SCO2 Have Regulatory Roles in the Maintenance of Cellular Copper Homeostasis Leary, Scot C.; Cobine, Paul A.; Kaufman, Brett A. Cell Metabolism, Vol. 5, Issue 1 https://doi.org/10.1016/j.cmet.2006.12.001	journal	January 2007
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
The Scoop on Sco Brière, Jean-Jacques; Tzagoloff, Alexander Molecular Cell, Vol. 25, Issue 2 https://doi.org/10.1016/j.molcel.2007.01.007	journal	January 2007
Solution Structure of Sco1 Balatri, Erica; Banci, Lucia; Bertini, Ivano Structure, Vol. 11, Issue 11 https://doi.org/10.1016/j.str.2003.10.004	journal	November 2003
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
Mutagenic Analysis of Cox11 of Rhodobacter sphaeroides : Insights into the Assembly of Cu _B of Cytochrome c Oxidase Thompson, Audie K.; Smith, Daniel; Gray, Jimmy Biochemistry, Vol. 49, Issue 27 https://doi.org/10.1021/bi1003876	journal	July 2010
From Redox Flow to Gene Regulation: Role of the PrrC Protein of Rhodobacter sphaeroides 2.4.1 ^† Eraso, Jesus M.; Kaplan, Samuel Biochemistry, Vol. 39, Issue 8 https://doi.org/10.1021/bi9923858	journal	February 2000
The Functions of Sco Proteins from Genome-Based Analysis Banci, Lucia; Bertini, Ivano; Cavallaro, Gabriele Journal of Proteome Research, Vol. 6, Issue 4 https://doi.org/10.1021/pr060538p	journal	April 2007
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
Versatile in vitro system to study translocation and functional integration of bacterial outer membrane proteins Norell, Derrick; Heuck, Alexander; Tran-Thi, Thuy-Anh Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6396	journal	November 2014
Periplasmic response upon disruption of transmembrane Cu transport in Pseudomonas aeruginosa Raimunda, Daniel; Padilla-Benavides, Teresita; Vogt, Stefan Metallomics, Vol. 5, Issue 2 https://doi.org/10.1039/c2mt20191g	journal	January 2013
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
Mechanism of Cu+-transporting ATPases: Soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites Gonzalez-Guerrero, M.; Arguello, J. M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 16 https://doi.org/10.1073/pnas.0711446105	journal	April 2008
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
Yeast Cox11, a Protein Essential for Cytochrome c Oxidase Assembly, Is a Cu(I)-binding Protein Carr, Heather S.; George, Graham N.; Winge, Dennis R. Journal of Biological Chemistry, Vol. 277, Issue 34 https://doi.org/10.1074/jbc.M204854200	journal	June 2002
Solution Structure of Cox11, a Novel Type of β-Immunoglobulin-like Fold Involved in Cu _B Site Formation of Cytochrome c Oxidase Banci, Lucia; Bertini, Ivano; Cantini, Francesca Journal of Biological Chemistry, Vol. 279, Issue 33 https://doi.org/10.1074/jbc.M403655200	journal	June 2004
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
Functional Analysis of the Domains in Cox11 Carr, Heather S.; Maxfield, Andrew B.; Horng, Yih-Chern Journal of Biological Chemistry, Vol. 280, Issue 24 https://doi.org/10.1074/jbc.M414077200	journal	April 2005
Mapping the Functional Interaction of Sco1 and Cox2 in Cytochrome Oxidase Biogenesis Rigby, Kevin; Cobine, Paul A.; Khalimonchuk, Oleh Journal of Biological Chemistry, Vol. 283, Issue 22 https://doi.org/10.1074/jbc.M710072200	journal	April 2008
Metal Transport across Biomembranes: Emerging Models for a Distinct Chemistry Argüello, José M.; Raimunda, Daniel; González-Guerrero, Manuel Journal of Biological Chemistry, Vol. 287, Issue 17 https://doi.org/10.1074/jbc.R111.319343	journal	March 2012
Redox Regulation of SCO Protein Function: Controlling Copper at a Mitochondrial Crossroad Leary, Scot C. Antioxidants & Redox Signaling, Vol. 13, Issue 9 https://doi.org/10.1089/ars.2010.3116	journal	November 2010
Deciphering protein-protein interactions during the biogenesis of cytochrome c oxidase from Paracoccus denitrificans Gurumoorthy, Priya; Ludwig, Bernd FEBS Journal, Vol. 282, Issue 3 https://doi.org/10.1111/febs.13160	journal	December 2014
Distinct functional roles of homologous Cu+ efflux ATPases in Pseudomonas aeruginosa: Role of Cu+ transport ATPases in Pseudomonas aeruginosa González-Guerrero, Manuel; Raimunda, Daniel; Cheng, Xin Molecular Microbiology, Vol. 78, Issue 5 https://doi.org/10.1111/j.1365-2958.2010.07402.x	journal	October 2010
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
Genetic Mutations Affecting the Respiratory Electron-Transport System of the Photosynthetic Bacterium Rhodopseudomonas capsulata Marrs, Barry; Gest, Howard Journal of Bacteriology, Vol. 114, Issue 3 https://doi.org/10.1128/JB.114.3.1045-1051.1973	journal	January 1973
Isolation and Characterization of Rhodobacter capsulatus Mutants Affected in Cytochromecbb 3 Oxidase Activity Koch, Hans-Georg; Hwang, Olivia; Daldal, Fevzi Journal of Bacteriology, Vol. 180, Issue 4 https://doi.org/10.1128/JB.180.4.969-978.1998	journal	January 1998
Involvement of SenC in Assembly of Cytochrome c Oxidase in Rhodobacter capsulatus Swem, D. L.; Swem, L. R.; Setterdahl, A. Journal of Bacteriology, Vol. 187, Issue 23 https://doi.org/10.1128/JB.187.23.8081-8087.2005	journal	November 2005
Formation of the Redox Cofactor Centers during Cox1 Maturation in Yeast Cytochrome Oxidase Khalimonchuk, O.; Bestwick, M.; Meunier, B. Molecular and Cellular Biology, Vol. 30, Issue 4 https://doi.org/10.1128/MCB.00640-09	journal	December 2009
Cytochrome c2-independent respiratory growth of Rhodobacter capsulatus. Daldal, F. Journal of Bacteriology, Vol. 170, Issue 5 https://doi.org/10.1128/jb.170.5.2388-2391.1988	journal	January 1988
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
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

Cited By (10)

Biochemical pathway for the biosynthesis of the Cu _A center in bacterial cytochrome c oxidase Canonica, Fabia; Hennecke, Hauke; Glockshuber, Rudi FEBS Letters, Vol. 593, Issue 21 https://doi.org/10.1002/1873-3468.13587	journal	July 2019
Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria Zhang, Yang; Blaby-Haas, Crysten E.; Steimle, Stefan Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37988-4	journal	February 2019
Handling of nutrient copper in the bacterial envelope Stewart, Louisa J.; Thaqi, Denis; Kobe, Bostjan Metallomics, Vol. 11, Issue 1 https://doi.org/10.1039/c8mt00218e	journal	January 2019
Transition metal transporters in rhizobia: tuning the inorganic micronutrient requirements to different living styles Abreu, Isidro; Mihelj, Paula; Raimunda, Daniel Metallomics, Vol. 11, Issue 4 https://doi.org/10.1039/c8mt00372f	journal	January 2019
PCu _A C domains from methane-oxidizing bacteria use a histidine brace to bind copper Fisher, Oriana S.; Sendzik, Madison R.; Ross, Matthew O. Journal of Biological Chemistry, Vol. 294, Issue 44 https://doi.org/10.1074/jbc.ra119.010093	journal	September 2019
Medicago truncatula copper transporter 1 (MtCOPT1) delivers copper for symbiotic nitrogen fixation Senovilla, Marta; Castro-Rodríguez, Rosario; Abreu, Isidro bioRxiv https://doi.org/10.1101/104554	posted_content	January 2017
The Cu chaperone CopZ is required for Cu homeostasis in Rhodobacter capsulatus and influences cytochrome cbb ₃ oxidase assembly : CopZ controls Cu homeostasis Utz, Marcel; Andrei, Andreea; Milanov, Martin Molecular Microbiology, Vol. 111, Issue 3 https://doi.org/10.1111/mmi.14190	journal	January 2019
Medicago truncatula copper transporter 1 (MtCOPT1) delivers copper for symbiotic nitrogen fixation Senovilla, Marta; Castro-Rodríguez, Rosario; Abreu, Isidro New Phytologist, Vol. 218, Issue 2 https://doi.org/10.1111/nph.14992	journal	January 2018
Structural basis and mechanism for metallochaperone-assisted assembly of the Cu _A center in cytochrome oxidase Canonica, Fabia; Klose, Daniel; Ledermann, Raphael Science Advances, Vol. 5, Issue 7 https://doi.org/10.1126/sciadv.aaw8478	journal	July 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

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

Journal Article · Mon Apr 02 20:00:00 EDT 2018 · ACS Chemical Biology · OSTI ID:1546085

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

Journal Article · Sun Dec 23 19:00:00 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 · Sun Sep 12 20:00:00 EDT 2021 · Frontiers in Microbiology · OSTI ID:1850003

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Rhodobacter capsulatus
cbb3-type cytochrome c oxidase biogenesis
copper homeostasis
periplasmic copper chaperones
respiration