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

Abstract

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 PCuAC-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.

Authors:
 [1];  [2];  [3];  [2];  [3];  [2]
+ Show Author Affiliations
  1. Institut fur Biochemie und Molekularbiologie, Freiburg (Germany); Albert-Ludwigs-Univ. Freiburg, Freiburg (Germany)
  2. Institut fur Biochemie und Molekularbiologie, Freiburg (Germany)
  3. Univ. of Pennsylvania, Philadelphia, PA (United States)
Publication Date:
Research Org.:
Univ. of Pennsylvania, Philadelphia, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1344916
Grant/Contract Number:  
FG02-91ER20052
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Microbiology
Additional Journal Information:
Journal Volume: 100; Journal Issue: 2; Journal ID: ISSN 0950-382X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cbb3-type cytochrome c oxidase biogenesis; periplasmic copper chaperones; copper homeostasis; respiration; Rhodobacter capsulatus

Citation Formats

Trasnea, Petru -Iulian, Utz, Marcel, Khalfaoui-Hassani, Bahia, Lagies, Simon, Daldal, Fevzi, and Koch, Hans -Georg. Cooperation between two periplasmic copper chaperones is required for full activity of the cbb3-type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus. United States: N. p., 2016. Web. doi:10.1111/mmi.13321.
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Trasnea, Petru -Iulian, Utz, Marcel, Khalfaoui-Hassani, Bahia, Lagies, Simon, Daldal, Fevzi, & Koch, Hans -Georg. Cooperation between two periplasmic copper chaperones is required for full activity of the cbb3-type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus. United States. https://doi.org/10.1111/mmi.13321
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Trasnea, Petru -Iulian, Utz, Marcel, Khalfaoui-Hassani, Bahia, Lagies, Simon, Daldal, Fevzi, and Koch, Hans -Georg. Sun . "Cooperation between two periplasmic copper chaperones is required for full activity of the cbb3-type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus". United States. https://doi.org/10.1111/mmi.13321. https://www.osti.gov/servlets/purl/1344916.
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@article{osti_1344916,
title = {Cooperation between two periplasmic copper chaperones is required for full activity of the cbb3-type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus},
author = {Trasnea, Petru -Iulian and Utz, Marcel and Khalfaoui-Hassani, Bahia and Lagies, Simon and Daldal, Fevzi and Koch, Hans -Georg},
abstractNote = {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 PCuAC-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.},
doi = {10.1111/mmi.13321},
journal = {Molecular Microbiology},
number = 2,
volume = 100,
place = {United States},
year = {Sun Feb 28 00:00:00 EST 2016},
month = {Sun Feb 28 00:00:00 EST 2016}
}
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https://doi.org/10.1111/mmi.13321
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    Works referencing / citing this record:

    Biochemical pathway for the biosynthesis of the Cu A center in bacterial cytochrome c oxidase
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    The Cu chaperone CopZ is required for Cu homeostasis in Rhodobacter capsulatus and influences cytochrome cbb 3 oxidase assembly : CopZ controls Cu homeostasis
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    Medicago truncatula copper transporter 1 (MtCOPT1) delivers copper for symbiotic nitrogen fixation
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    Structural basis and mechanism for metallochaperone-assisted assembly of the CuA center in cytochrome oxidase
    text, January 2019

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