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Title: The Escherichia coli MFS-type transporter genes yhjE, ydiM, and yfcJ are required to produce an active bo3 quinol oxidase

Abstract

Heme-copper oxygen reductases are membrane-bound oligomeric complexes that are integral to prokaryotic and eukaryotic aerobic respiratory chains. Biogenesis of these enzymes is complex and requires coordinated assembly of the subunits and their cofactors. Some of the components are involved in the acquisition and integration of different heme and copper (Cu) cofactors into these terminal oxygen reductases. As such, MFS-type transporters of the CalT family ( e . g ., CcoA) are required for Cu import and heme-Cu B center biogenesis of the cbb 3 -type cytochrome c oxidases ( cbb 3 -Cox). However, functionally homologous Cu transporters for similar heme-Cu containing bo 3 -type quinol oxidases ( bo 3 -Qox) are unknown. Despite the occurrence of multiple MFS-type transporters, orthologs of CcoA are absent in bacteria like Escherichia coli that contain bo 3 -Qox. In this work, we identified a subset of uncharacterized MFS transporters, based on the presence of putative metal-binding residues, as likely candidates for the missing Cu transporter. Using a genetic approach, we tested whether these transporters are involved in the biogenesis of E . coli bo 3 -Qox. When respiratory growth is dependent on bo 3 -Qox, because of deletion of the bd -type Qox enzymes,more » three candidate genes, yhjE , ydiM , and yfcJ , were found to be critical for E . coli growth. Radioactive metal uptake assays showed that Δ ydiM has a slower 64 Cu uptake, whereas Δ yhjE accumulates reduced 55 Fe in the cell, while no similar uptake defect is associated with Δ ycfJ . Phylogenomic analyses suggest plausible roles for the YhjE, YdiM, and YfcJ transporters, and overall findings illustrate the diverse roles that the MFS-type transporters play in cellular metal homeostasis and production of active heme-Cu oxygen reductases.« less

Authors:
; ; ; ;
Publication Date:
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
2203132
Grant/Contract Number:  
FG02-91ER20052; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 18 Journal Issue: 10; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English

Citation Formats

Khalfaoui-Hassani, Bahia, Blaby-Haas, Crysten E., Verissimo, Andreia, Daldal, Fevzi, and Mapder, ed., Tarunendu. The Escherichia coli MFS-type transporter genes yhjE, ydiM, and yfcJ are required to produce an active bo3 quinol oxidase. United States: N. p., 2023. Web. doi:10.1371/journal.pone.0293015.
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Khalfaoui-Hassani, Bahia, Blaby-Haas, Crysten E., Verissimo, Andreia, Daldal, Fevzi, & Mapder, ed., Tarunendu. The Escherichia coli MFS-type transporter genes yhjE, ydiM, and yfcJ are required to produce an active bo3 quinol oxidase. United States. https://doi.org/10.1371/journal.pone.0293015
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Khalfaoui-Hassani, Bahia, Blaby-Haas, Crysten E., Verissimo, Andreia, Daldal, Fevzi, and Mapder, ed., Tarunendu. Fri . "The Escherichia coli MFS-type transporter genes yhjE, ydiM, and yfcJ are required to produce an active bo3 quinol oxidase". United States. https://doi.org/10.1371/journal.pone.0293015.
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@article{osti_2203132,
title = {The Escherichia coli MFS-type transporter genes yhjE, ydiM, and yfcJ are required to produce an active bo3 quinol oxidase},
author = {Khalfaoui-Hassani, Bahia and Blaby-Haas, Crysten E. and Verissimo, Andreia and Daldal, Fevzi and Mapder, ed., Tarunendu},
abstractNote = {Heme-copper oxygen reductases are membrane-bound oligomeric complexes that are integral to prokaryotic and eukaryotic aerobic respiratory chains. Biogenesis of these enzymes is complex and requires coordinated assembly of the subunits and their cofactors. Some of the components are involved in the acquisition and integration of different heme and copper (Cu) cofactors into these terminal oxygen reductases. As such, MFS-type transporters of the CalT family ( e . g ., CcoA) are required for Cu import and heme-Cu B center biogenesis of the cbb 3 -type cytochrome c oxidases ( cbb 3 -Cox). However, functionally homologous Cu transporters for similar heme-Cu containing bo 3 -type quinol oxidases ( bo 3 -Qox) are unknown. Despite the occurrence of multiple MFS-type transporters, orthologs of CcoA are absent in bacteria like Escherichia coli that contain bo 3 -Qox. In this work, we identified a subset of uncharacterized MFS transporters, based on the presence of putative metal-binding residues, as likely candidates for the missing Cu transporter. Using a genetic approach, we tested whether these transporters are involved in the biogenesis of E . coli bo 3 -Qox. When respiratory growth is dependent on bo 3 -Qox, because of deletion of the bd -type Qox enzymes, three candidate genes, yhjE , ydiM , and yfcJ , were found to be critical for E . coli growth. Radioactive metal uptake assays showed that Δ ydiM has a slower 64 Cu uptake, whereas Δ yhjE accumulates reduced 55 Fe in the cell, while no similar uptake defect is associated with Δ ycfJ . Phylogenomic analyses suggest plausible roles for the YhjE, YdiM, and YfcJ transporters, and overall findings illustrate the diverse roles that the MFS-type transporters play in cellular metal homeostasis and production of active heme-Cu oxygen reductases.},
doi = {10.1371/journal.pone.0293015},
journal = {PLoS ONE},
number = 10,
volume = 18,
place = {United States},
year = {Fri Oct 20 00:00:00 EDT 2023},
month = {Fri Oct 20 00:00:00 EDT 2023}
}
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