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The CopA2-Type P1B-Type ATPase CcoI Serves as Central Hub for cbb3-Type Cytochrome Oxidase Biogenesis

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [3];  [3];  [3];  [4];  [3];  [5];  [4];  [3]
  1. Albert-Ludwigs-Universität Freiburg (Germany). Faculty of Medicine. ZBMZ. Institut für Biochemie und Molekularbiologie; Albert-Ludwigs-Universität Freiburg (Germany). Faculty of Biology; Albert-Ludwigs-Universität Freiburg (Germany)
  2. Albert-Ludwigs-Universität Freiburg (Germany). Faculty of Chemistry and Pharmacy. Inst. for Biochemistry; Univ. of Freiburg (Germany). Spemann Graduate School of Biology and Medicine (SGBM); Albert-Ludwigs-Universität Freiburg (Germany). Faculty of Chemistry and Pharmacy
  3. Albert-Ludwigs-Universität Freiburg (Germany). Faculty of Medicine. ZBMZ. Institut für Biochemie und Molekularbiologie
  4. Albert-Ludwigs-Universität Freiburg (Germany). Faculty of Chemistry and Pharmacy. Inst. for Biochemistry
  5. Univ. of Pennsylvania, Philadelphia, PA (United States). Dept. of Biology
+ Show Author Affiliations
Copper (Cu)-transporting P1B-type ATPases are ubiquitous metal transporters and crucial for maintaining Cu homeostasis in all domains of life. In bacteria, the P1B-type ATPase CopA is required for Cu-detoxification and exports excess Cu(I) in an ATP-dependent reaction from the cytosol into the periplasm. CopA is a member of the CopA1-type ATPase family and has been biochemically and structurally characterized in detail. In contrast, less is known about members of the CopA2-type ATPase family, which are predicted to transport Cu(I) into the periplasm for cuproprotein maturation. One example is CcoI, which is required for the maturation of cbb3-type cytochrome oxidase (cbb3-Cox) in different species. Here, we reconstituted purified CcoI of Rhodobacter capsulatus into liposomes and determined Cu transport using solid-supported membrane electrophysiology. The data demonstrate ATP-dependent Cu(I) translocation by CcoI, while no transport is observed in the presence of a non-hydrolysable ATP analog. CcoI contains two cytosolically exposed N-terminal metal binding sites (N-MBSs), which are both important, but not essential for Cu delivery to cbb3-Cox. CcoI and cbb3-Cox activity assays in the presence of different Cu concentrations suggest that the glutaredoxin-like N-MBS1 is primarily involved in regulating the ATPase activity of CcoI, while the CopZ-like N-MBS2 is involved in Cu(I) acquisition. The interaction of CcoI with periplasmic Cu chaperones was analyzed by genetically fusing CcoI to the chaperone SenC. The CcoI-SenC fusion protein was fully functional in vivo and sufficient to provide Cu for cbb3-Cox maturation. In summary, our data demonstrate that CcoI provides the link between the cytosolic and periplasmic Cu chaperone networks during cbb3-Cox assembly.
Research Organization:
Univ. of Pennsylvania, Philadelphia, PA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); German Research Foundation (DFG); National Institutes of Health (NIH)
Grant/Contract Number:
FG02-91ER20052
OSTI ID:
1850003
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 12; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

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59 BASIC BIOLOGICAL SCIENCES
CcoI
CopZ
P1B-type ATPases
Rhodobacter capsulatus
SenC
cbb3-type cytochrome c oxidase biogenesis
microbiology
solid-supported membrane electrophysiology