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Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation

In F(o)F(1)-ATP synthase, proton translocation through F(o) drives rotation of the c-subunit oligomeric ring relative to the a-subunit. Recent studies suggest that in each step of the rotation, key glutamic acid residues in different c-subunits contribute to proton release to and proton uptake from...

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Autores principales: Mitome, Noriyo, Kubo, Shintaroh, Ohta, Sumie, Takashima, Hikaru, Shigefuji, Yuto, Niina, Toru, Takada, Shoji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8809890/
https://www.ncbi.nlm.nih.gov/pubmed/35107420
http://dx.doi.org/10.7554/eLife.69096
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author Mitome, Noriyo
Kubo, Shintaroh
Ohta, Sumie
Takashima, Hikaru
Shigefuji, Yuto
Niina, Toru
Takada, Shoji
author_facet Mitome, Noriyo
Kubo, Shintaroh
Ohta, Sumie
Takashima, Hikaru
Shigefuji, Yuto
Niina, Toru
Takada, Shoji
author_sort Mitome, Noriyo
collection PubMed
description In F(o)F(1)-ATP synthase, proton translocation through F(o) drives rotation of the c-subunit oligomeric ring relative to the a-subunit. Recent studies suggest that in each step of the rotation, key glutamic acid residues in different c-subunits contribute to proton release to and proton uptake from the a-subunit. However, no studies have demonstrated cooperativity among c-subunits toward F(o)F(1)-ATP synthase activity. Here, we addressed this using Bacillus PS3 ATP synthase harboring a c-ring with various combinations of wild-type and cE56D, enabled by genetically fused single-chain c-ring. ATP synthesis and proton pump activities were decreased by a single cE56D mutation and further decreased by double cE56D mutations. Moreover, activity further decreased as the two mutation sites were separated, indicating cooperation among c-subunits. Similar results were obtained for proton transfer-coupled molecular simulations. The simulations revealed that prolonged proton uptake in mutated c-subunits is shared between two c-subunits, explaining the cooperation observed in biochemical assays.
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spelling pubmed-88098902022-02-04 Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation Mitome, Noriyo Kubo, Shintaroh Ohta, Sumie Takashima, Hikaru Shigefuji, Yuto Niina, Toru Takada, Shoji eLife Biochemistry and Chemical Biology In F(o)F(1)-ATP synthase, proton translocation through F(o) drives rotation of the c-subunit oligomeric ring relative to the a-subunit. Recent studies suggest that in each step of the rotation, key glutamic acid residues in different c-subunits contribute to proton release to and proton uptake from the a-subunit. However, no studies have demonstrated cooperativity among c-subunits toward F(o)F(1)-ATP synthase activity. Here, we addressed this using Bacillus PS3 ATP synthase harboring a c-ring with various combinations of wild-type and cE56D, enabled by genetically fused single-chain c-ring. ATP synthesis and proton pump activities were decreased by a single cE56D mutation and further decreased by double cE56D mutations. Moreover, activity further decreased as the two mutation sites were separated, indicating cooperation among c-subunits. Similar results were obtained for proton transfer-coupled molecular simulations. The simulations revealed that prolonged proton uptake in mutated c-subunits is shared between two c-subunits, explaining the cooperation observed in biochemical assays. eLife Sciences Publications, Ltd 2022-02-02 /pmc/articles/PMC8809890/ /pubmed/35107420 http://dx.doi.org/10.7554/eLife.69096 Text en © 2022, Mitome et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Biochemistry and Chemical Biology
Mitome, Noriyo
Kubo, Shintaroh
Ohta, Sumie
Takashima, Hikaru
Shigefuji, Yuto
Niina, Toru
Takada, Shoji
Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation
title Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation
title_full Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation
title_fullStr Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation
title_full_unstemmed Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation
title_short Cooperation among c-subunits of F(o)F(1)-ATP synthase in rotation-coupled proton translocation
title_sort cooperation among c-subunits of f(o)f(1)-atp synthase in rotation-coupled proton translocation
topic Biochemistry and Chemical Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8809890/
https://www.ncbi.nlm.nih.gov/pubmed/35107420
http://dx.doi.org/10.7554/eLife.69096
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