Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases

Khalfaoui-Hassani, Bahia; Wu, Hongjiang; Blaby-Haas, Crysten E.; Zhang, Yang; Sandri, Federica; Verissimo, Andreia F.; Koch, Hans-Georg; Daldal, Fevzi

doi:10.1128/mBio.00065-18

Title: Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases

Journal Article · Tue Feb 27 00:00:00 EST 2018 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.00065-18· OSTI ID:1422646

Khalfaoui-Hassani, Bahia ^[1]; Wu, Hongjiang ^[2]; Blaby-Haas, Crysten E. ^[3]; Zhang, Yang ^[2]; Sandri, Federica ^[2]; Verissimo, Andreia F. ^[2]; Koch, Hans-Georg ^[4]; Daldal, Fevzi ^[2]

Univ. of Pennsylvania, Philadelphia, PA (United States). Dept. of Biology; Univ. of Pau and Pays de l'Adour, Pau (France). Faculty of Environmental Microbiology and Inst. of Analytical Sciences and Physico-Chemistry for Environment and Materials (IPREM)
Univ. of Pennsylvania, Philadelphia, PA (United States). Dept. of Biology
Brookhaven National Lab. (BNL), Upton, NY (United States). Biology Dept.
Albert Ludwigs Univ. of Freiburg, Freiburg (Germany). Inst. for Biochemistry and Molecular Biology and Center for Biochemistry and Molecular Cell Research (ZBMZ) and Faculty of Medicine

ABSTRACT Cytochromecoxidases are members of the heme-copper oxidase superfamily. These enzymes have different subunits, cofactors, and primary electron acceptors, yet they all contain identical heme-copper (Cu_B) binuclear centers within their catalytic subunits. The uptake and delivery pathways of the Cu_Batom incorporated into this active site, where oxygen is reduced to water, are not well understood. Our previous work with the facultative phototrophic bacteriumRhodobacter capsulatusindicated that the copper atom needed for the Cu_Bsite ofcbb₃-type cytochromecoxidase (cbb₃-Cox) is imported to the cytoplasm by a major facilitator superfamily-type transporter, CcoA. In this study, a comparative genomic analysis of CcoA orthologs in alphaproteobacterial genomes showed that CcoA is widespread among organisms and frequently co-occurs with cytochromecoxidases. To define the specificity of CcoA activity, we investigated its function inRhodobacter sphaeroides, a close relative ofR. capsulatusthat contains bothcbb₃- andaa₃-Cox. Phenotypic, genetic, and biochemical characterization of mutants lacking CcoA showed that in its absence, or even in the presence of its bypass suppressors, only the production ofcbb₃-Cox and not that ofaa₃-Cox was affected. We therefore concluded that CcoA is dedicated solely tocbb₃-Cox biogenesis, establishing that distinct copper uptake systems provide the Cu_Batoms to the catalytic sites of these two similar cytochromecoxidases. These findings illustrate the large variety of strategies that organisms employ to ensure homeostasis and fine control of copper trafficking and delivery to the target cuproproteins under different physiological conditions. IMPORTANCEThecbb₃- andaa₃-type cytochromecoxidases belong to the widespread heme-copper oxidase superfamily. They are membrane-integral cuproproteins that catalyze oxygen reduction to water under hypoxic and normoxic growth conditions. These enzymes diverge in terms of subunit and cofactor composition, yet they all share a conserved heme-copper binuclear site within their catalytic subunit. In this study, we show that the copper atoms of the catalytic center of two similar cytochromecoxidases from this superfamily are provided by different copper uptake systems during their biogenesis. This finding illustrates different strategies by which organisms fine-tune the trafficking of copper, which is an essential but toxic micronutrient.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH); German Research Foundation (DFG)

Grant/Contract Number:: SC0012704; FG02-91ER20052; 38237; IRTG 1478; RTG 2202

OSTI ID:: 1422646

Alternate ID(s):: OSTI ID: 1426445

Report Number(s):: BNL-203362-2018-JAAM; e00065-18

Journal Information:: mBio (Online), Journal Name: mBio (Online) Vol. 9 Journal Issue: 1; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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59 BASIC BIOLOGICAL SCIENCES
CcoA
cytochrome
copper homeostasis
copper transport
copper uptake
cytochrome biogenesis
cytochrome c oxidase

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