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Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation

Arc (anoxic redox control), one of the most intensely investigated two-component regulatory systems in γ-proteobacteria, plays a major role in mediating the metabolic transition from aerobiosis to anaerobiosis. In Shewanella oneidensis, a research model for respiratory versatility, Arc is crucial fo...

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Autores principales: Xie, Peilu, Wang, Jiahao, Liang, Huihui, Gao, Haichun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8470723/
https://www.ncbi.nlm.nih.gov/pubmed/34575075
http://dx.doi.org/10.3390/life11090926
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author Xie, Peilu
Wang, Jiahao
Liang, Huihui
Gao, Haichun
author_facet Xie, Peilu
Wang, Jiahao
Liang, Huihui
Gao, Haichun
author_sort Xie, Peilu
collection PubMed
description Arc (anoxic redox control), one of the most intensely investigated two-component regulatory systems in γ-proteobacteria, plays a major role in mediating the metabolic transition from aerobiosis to anaerobiosis. In Shewanella oneidensis, a research model for respiratory versatility, Arc is crucial for aerobic growth. However, how this occurs remains largely unknown. In this study, we demonstrated that the loss of the response regulator ArcA distorts the correlation between transcription and translation by inhibiting the ribosome biosynthesis. This effect largely underlies the growth defect because it concurs with the effect of chloramphenicol, which impairs translation. Reduced transcription of ArcA-dependent ribosomal protein S1 appears to have a significant impact on ribosome assembly. We further show that the lowered translation efficiency is not accountable for the envelope defect, another major defect resulting from the ArcA loss. Overall, our results suggest that although the arcA mutation impairs growth through multi-fold complex impacts in physiology, the reduced translation efficacy appears to be a major cause for the phenotype, demonstrating that Arc is a primary system that coordinates proteomic resources with metabolism in S. oneidensis.
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spelling pubmed-84707232021-09-27 Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation Xie, Peilu Wang, Jiahao Liang, Huihui Gao, Haichun Life (Basel) Article Arc (anoxic redox control), one of the most intensely investigated two-component regulatory systems in γ-proteobacteria, plays a major role in mediating the metabolic transition from aerobiosis to anaerobiosis. In Shewanella oneidensis, a research model for respiratory versatility, Arc is crucial for aerobic growth. However, how this occurs remains largely unknown. In this study, we demonstrated that the loss of the response regulator ArcA distorts the correlation between transcription and translation by inhibiting the ribosome biosynthesis. This effect largely underlies the growth defect because it concurs with the effect of chloramphenicol, which impairs translation. Reduced transcription of ArcA-dependent ribosomal protein S1 appears to have a significant impact on ribosome assembly. We further show that the lowered translation efficiency is not accountable for the envelope defect, another major defect resulting from the ArcA loss. Overall, our results suggest that although the arcA mutation impairs growth through multi-fold complex impacts in physiology, the reduced translation efficacy appears to be a major cause for the phenotype, demonstrating that Arc is a primary system that coordinates proteomic resources with metabolism in S. oneidensis. MDPI 2021-09-06 /pmc/articles/PMC8470723/ /pubmed/34575075 http://dx.doi.org/10.3390/life11090926 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Xie, Peilu
Wang, Jiahao
Liang, Huihui
Gao, Haichun
Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation
title Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation
title_full Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation
title_fullStr Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation
title_full_unstemmed Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation
title_short Shewanella oneidensis arcA Mutation Impairs Aerobic Growth Mainly by Compromising Translation
title_sort shewanella oneidensis arca mutation impairs aerobic growth mainly by compromising translation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8470723/
https://www.ncbi.nlm.nih.gov/pubmed/34575075
http://dx.doi.org/10.3390/life11090926
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