The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.

The arsenite oxidase (Aio) from the facultative autotrophic Alphaproteobacterium Rhizobium sp. NT-26 is a bioenergetic enzyme involved in the oxidation of arsenite to arsenate. The enzyme from the distantly related heterotroph, Alcaligenes faecalis, which is thought to oxidise arsenite for detoxific...

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Main Authors: Thomas P Warelow, Muse Oke, Barbara Schoepp-Cothenet, Jan U Dahl, Nicole Bruselat, Ganesh N Sivalingam, Silke Leimkühler, Konstantinos Thalassinos, Ulrike Kappler, James H Naismith, Joanne M Santini
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0072535
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author Thomas P Warelow
Muse Oke
Barbara Schoepp-Cothenet
Jan U Dahl
Nicole Bruselat
Ganesh N Sivalingam
Silke Leimkühler
Konstantinos Thalassinos
Ulrike Kappler
James H Naismith
Joanne M Santini
author_facet Thomas P Warelow
Muse Oke
Barbara Schoepp-Cothenet
Jan U Dahl
Nicole Bruselat
Ganesh N Sivalingam
Silke Leimkühler
Konstantinos Thalassinos
Ulrike Kappler
James H Naismith
Joanne M Santini
author_sort Thomas P Warelow
collection DOAJ
description The arsenite oxidase (Aio) from the facultative autotrophic Alphaproteobacterium Rhizobium sp. NT-26 is a bioenergetic enzyme involved in the oxidation of arsenite to arsenate. The enzyme from the distantly related heterotroph, Alcaligenes faecalis, which is thought to oxidise arsenite for detoxification, consists of a large α subunit (AioA) with bis-molybdopterin guanine dinucleotide at its active site and a 3Fe-4S cluster, and a small β subunit (AioB) which contains a Rieske 2Fe-2S cluster. The successful heterologous expression of the NT-26 Aio in Escherichia coli has resulted in the solution of its crystal structure. The NT-26 Aio, a heterotetramer, shares high overall similarity to the heterodimeric arsenite oxidase from A. faecalis but there are striking differences in the structure surrounding the Rieske 2Fe-2S cluster which we demonstrate explains the difference in the observed redox potentials (+225 mV vs. +130/160 mV, respectively). A combination of site-directed mutagenesis and electron paramagnetic resonance was used to explore the differences observed in the structure and redox properties of the Rieske cluster. In the NT-26 AioB the substitution of a serine (S126 in NT-26) for a threonine as in the A. faecalis AioB explains a -20 mV decrease in redox potential. The disulphide bridge in the A. faecalis AioB which is conserved in other betaproteobacterial AioB subunits and the Rieske subunit of the cytochrome bc 1 complex is absent in the NT-26 AioB subunit. The introduction of a disulphide bridge had no effect on Aio activity or protein stability but resulted in a decrease in the redox potential of the cluster. These results are in conflict with previous data on the betaproteobacterial AioB subunit and the Rieske of the bc 1 complex where removal of the disulphide bridge had no effect on the redox potential of the former but a decrease in cluster stability was observed in the latter.
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spelling doaj-art-080c252a643540bda2f9abc0330de0102025-08-20T02:22:45ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0188e7253510.1371/journal.pone.0072535The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.Thomas P WarelowMuse OkeBarbara Schoepp-CothenetJan U DahlNicole BruselatGanesh N SivalingamSilke LeimkühlerKonstantinos ThalassinosUlrike KapplerJames H NaismithJoanne M SantiniThe arsenite oxidase (Aio) from the facultative autotrophic Alphaproteobacterium Rhizobium sp. NT-26 is a bioenergetic enzyme involved in the oxidation of arsenite to arsenate. The enzyme from the distantly related heterotroph, Alcaligenes faecalis, which is thought to oxidise arsenite for detoxification, consists of a large α subunit (AioA) with bis-molybdopterin guanine dinucleotide at its active site and a 3Fe-4S cluster, and a small β subunit (AioB) which contains a Rieske 2Fe-2S cluster. The successful heterologous expression of the NT-26 Aio in Escherichia coli has resulted in the solution of its crystal structure. The NT-26 Aio, a heterotetramer, shares high overall similarity to the heterodimeric arsenite oxidase from A. faecalis but there are striking differences in the structure surrounding the Rieske 2Fe-2S cluster which we demonstrate explains the difference in the observed redox potentials (+225 mV vs. +130/160 mV, respectively). A combination of site-directed mutagenesis and electron paramagnetic resonance was used to explore the differences observed in the structure and redox properties of the Rieske cluster. In the NT-26 AioB the substitution of a serine (S126 in NT-26) for a threonine as in the A. faecalis AioB explains a -20 mV decrease in redox potential. The disulphide bridge in the A. faecalis AioB which is conserved in other betaproteobacterial AioB subunits and the Rieske subunit of the cytochrome bc 1 complex is absent in the NT-26 AioB subunit. The introduction of a disulphide bridge had no effect on Aio activity or protein stability but resulted in a decrease in the redox potential of the cluster. These results are in conflict with previous data on the betaproteobacterial AioB subunit and the Rieske of the bc 1 complex where removal of the disulphide bridge had no effect on the redox potential of the former but a decrease in cluster stability was observed in the latter.https://doi.org/10.1371/journal.pone.0072535
spellingShingle Thomas P Warelow
Muse Oke
Barbara Schoepp-Cothenet
Jan U Dahl
Nicole Bruselat
Ganesh N Sivalingam
Silke Leimkühler
Konstantinos Thalassinos
Ulrike Kappler
James H Naismith
Joanne M Santini
The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.
PLoS ONE
title The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.
title_full The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.
title_fullStr The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.
title_full_unstemmed The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.
title_short The respiratory arsenite oxidase: structure and the role of residues surrounding the rieske cluster.
title_sort respiratory arsenite oxidase structure and the role of residues surrounding the rieske cluster
url https://doi.org/10.1371/journal.pone.0072535
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