Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases

ABSTRACT Cytochrome c oxidases 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 (CuB) binuclear centers within their catalytic subunits. The uptake and delivery pathways of...

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Autores principales:	Bahia Khalfaoui-Hassani, Hongjiang Wu, Crysten E. Blaby-Haas, Yang Zhang, Federica Sandri, Andreia F. Verissimo, Hans-Georg Koch, Fevzi Daldal
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	CcoA cytochrome copper homeostasis copper transport copper uptake cytochrome biogenesis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/927e4afdd3134bba8a21cd41d1d3ba94
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spelling	oai:doaj.org-article:927e4afdd3134bba8a21cd41d1d3ba942021-11-15T15:53:26ZWidespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases10.1128/mBio.00065-182150-7511https://doaj.org/article/927e4afdd3134bba8a21cd41d1d3ba942018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00065-18https://doaj.org/toc/2150-7511ABSTRACT Cytochrome c oxidases 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 (CuB) binuclear centers within their catalytic subunits. The uptake and delivery pathways of the CuB atom incorporated into this active site, where oxygen is reduced to water, are not well understood. Our previous work with the facultative phototrophic bacterium Rhodobacter capsulatus indicated that the copper atom needed for the CuB site of cbb3-type cytochrome c oxidase (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 cytochrome c oxidases. To define the specificity of CcoA activity, we investigated its function in Rhodobacter sphaeroides, a close relative of R. capsulatus that contains both cbb3- and aa3-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 of cbb3-Cox and not that of aa3-Cox was affected. We therefore concluded that CcoA is dedicated solely to cbb3-Cox biogenesis, establishing that distinct copper uptake systems provide the CuB atoms to the catalytic sites of these two similar cytochrome c oxidases. 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. IMPORTANCE The cbb3- and aa3-type cytochrome c oxidases 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 cytochrome c oxidases 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.Bahia Khalfaoui-HassaniHongjiang WuCrysten E. Blaby-HaasYang ZhangFederica SandriAndreia F. VerissimoHans-Georg KochFevzi DaldalAmerican Society for MicrobiologyarticleCcoAcytochromecopper homeostasiscopper transportcopper uptakecytochrome biogenesisMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	CcoA cytochrome copper homeostasis copper transport copper uptake cytochrome biogenesis Microbiology QR1-502
spellingShingle	CcoA cytochrome copper homeostasis copper transport copper uptake cytochrome biogenesis Microbiology QR1-502 Bahia Khalfaoui-Hassani Hongjiang Wu Crysten E. Blaby-Haas Yang Zhang Federica Sandri Andreia F. Verissimo Hans-Georg Koch Fevzi Daldal Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases
description	ABSTRACT Cytochrome c oxidases 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 (CuB) binuclear centers within their catalytic subunits. The uptake and delivery pathways of the CuB atom incorporated into this active site, where oxygen is reduced to water, are not well understood. Our previous work with the facultative phototrophic bacterium Rhodobacter capsulatus indicated that the copper atom needed for the CuB site of cbb3-type cytochrome c oxidase (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 cytochrome c oxidases. To define the specificity of CcoA activity, we investigated its function in Rhodobacter sphaeroides, a close relative of R. capsulatus that contains both cbb3- and aa3-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 of cbb3-Cox and not that of aa3-Cox was affected. We therefore concluded that CcoA is dedicated solely to cbb3-Cox biogenesis, establishing that distinct copper uptake systems provide the CuB atoms to the catalytic sites of these two similar cytochrome c oxidases. 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. IMPORTANCE The cbb3- and aa3-type cytochrome c oxidases 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 cytochrome c oxidases 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.
format	article
author	Bahia Khalfaoui-Hassani Hongjiang Wu Crysten E. Blaby-Haas Yang Zhang Federica Sandri Andreia F. Verissimo Hans-Georg Koch Fevzi Daldal
author_facet	Bahia Khalfaoui-Hassani Hongjiang Wu Crysten E. Blaby-Haas Yang Zhang Federica Sandri Andreia F. Verissimo Hans-Georg Koch Fevzi Daldal
author_sort	Bahia Khalfaoui-Hassani
title	Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases
title_short	Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases
title_full	Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases
title_fullStr	Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases
title_full_unstemmed	Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases
title_sort	widespread distribution and functional specificity of the copper importer ccoa: distinct cu uptake routes for bacterial cytochrome <italic toggle="yes">c</italic> oxidases
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/927e4afdd3134bba8a21cd41d1d3ba94
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Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome <italic toggle="yes">c</italic> Oxidases

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