Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>

ABSTRACT The acquisition, delivery, and incorporation of metals into their respective metalloproteins are important cellular processes. These processes are tightly controlled in order to prevent exposure of cells to free-metal concentrations that could yield oxidative damage. Copper (Cu) is one such...

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Autores principales:	Seda Ekici, Honghui Yang, Hans-Georg Koch, Fevzi Daldal
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cf7c642134e4456ead95752f1d3a7d88
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spelling	oai:doaj.org-article:cf7c642134e4456ead95752f1d3a7d882021-11-15T15:39:02ZNovel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>10.1128/mBio.00293-112150-7511https://doaj.org/article/cf7c642134e4456ead95752f1d3a7d882012-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00293-11https://doaj.org/toc/2150-7511ABSTRACT The acquisition, delivery, and incorporation of metals into their respective metalloproteins are important cellular processes. These processes are tightly controlled in order to prevent exposure of cells to free-metal concentrations that could yield oxidative damage. Copper (Cu) is one such metal that is required as a cofactor in a variety of proteins. However, when present in excessive amounts, Cu is toxic due to its oxidative capability. Cytochrome c oxidases (Coxs) are among the metalloproteins whose assembly and activity require the presence of Cu in their catalytic subunits. In this study, we focused on the acquisition of Cu for incorporation into the heme-Cu binuclear center of the cbb3-type Cox (cbb3-Cox) in the facultative phototroph Rhodobacter capsulatus. Genetic screens identified a cbb3-Cox defective mutant that requires Cu2+ supplementation to produce an active cbb3-Cox. Complementation of this mutant using wild-type genomic libraries unveiled a novel gene (ccoA) required for cbb3-Cox biogenesis. In the absence of CcoA, the cellular Cu content decreases and cbb3-Cox assembly and activity become defective. CcoA shows homology to major facilitator superfamily (MFS)-type transporter proteins. Members of this family are known to transport small solutes or drugs, but so far, no MFS protein has been implicated in cbb3-Cox biogenesis. These findings provide novel insights into the maturation and assembly of membrane-integral metalloproteins and on a hitherto-unknown function(s) of MFS-type transporters in bacterial Cu acquisition. IMPORTANCE Biogenesis of energy-transducing membrane-integral enzymes, like the heme copper-containing cytochrome c oxidases, and the acquisition of transition metals, like copper, as their catalytic cofactors are vital processes for all cells. These widespread and well-controlled processes are poorly understood in all organisms, including bacteria. Defects in these processes lead to severe mitochondrial diseases in humans and poor crop yields in plants. In this study, using the facultative phototroph Rhodobacter capsulatus as a model organism, we report on the discovery of a novel major facilitator superfamily (MFS)-type transporter (CcoA) that affects cellular copper content and cbb3-type cytochrome c oxidase production in bacteria.Seda EkiciHonghui YangHans-Georg KochFevzi DaldalAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 1 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Seda Ekici Honghui Yang Hans-Georg Koch Fevzi Daldal Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>
description	ABSTRACT The acquisition, delivery, and incorporation of metals into their respective metalloproteins are important cellular processes. These processes are tightly controlled in order to prevent exposure of cells to free-metal concentrations that could yield oxidative damage. Copper (Cu) is one such metal that is required as a cofactor in a variety of proteins. However, when present in excessive amounts, Cu is toxic due to its oxidative capability. Cytochrome c oxidases (Coxs) are among the metalloproteins whose assembly and activity require the presence of Cu in their catalytic subunits. In this study, we focused on the acquisition of Cu for incorporation into the heme-Cu binuclear center of the cbb3-type Cox (cbb3-Cox) in the facultative phototroph Rhodobacter capsulatus. Genetic screens identified a cbb3-Cox defective mutant that requires Cu2+ supplementation to produce an active cbb3-Cox. Complementation of this mutant using wild-type genomic libraries unveiled a novel gene (ccoA) required for cbb3-Cox biogenesis. In the absence of CcoA, the cellular Cu content decreases and cbb3-Cox assembly and activity become defective. CcoA shows homology to major facilitator superfamily (MFS)-type transporter proteins. Members of this family are known to transport small solutes or drugs, but so far, no MFS protein has been implicated in cbb3-Cox biogenesis. These findings provide novel insights into the maturation and assembly of membrane-integral metalloproteins and on a hitherto-unknown function(s) of MFS-type transporters in bacterial Cu acquisition. IMPORTANCE Biogenesis of energy-transducing membrane-integral enzymes, like the heme copper-containing cytochrome c oxidases, and the acquisition of transition metals, like copper, as their catalytic cofactors are vital processes for all cells. These widespread and well-controlled processes are poorly understood in all organisms, including bacteria. Defects in these processes lead to severe mitochondrial diseases in humans and poor crop yields in plants. In this study, using the facultative phototroph Rhodobacter capsulatus as a model organism, we report on the discovery of a novel major facilitator superfamily (MFS)-type transporter (CcoA) that affects cellular copper content and cbb3-type cytochrome c oxidase production in bacteria.
format	article
author	Seda Ekici Honghui Yang Hans-Georg Koch Fevzi Daldal
author_facet	Seda Ekici Honghui Yang Hans-Georg Koch Fevzi Daldal
author_sort	Seda Ekici
title	Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>
title_short	Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>
title_full	Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>
title_fullStr	Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>
title_full_unstemmed	Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>
title_sort	novel transporter required for biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-type cytochrome <italic toggle="yes">c</italic> oxidase in <named-content content-type="genus-species">rhodobacter capsulatus</named-content>
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/cf7c642134e4456ead95752f1d3a7d88
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Novel Transporter Required for Biogenesis of <italic toggle="yes">cbb</italic><sub>3</sub>-Type Cytochrome <italic toggle="yes">c</italic> Oxidase in <named-content content-type="genus-species">Rhodobacter capsulatus</named-content>

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