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Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification

More than half of the protein-coding genes in bacteria are organized in polycistronic operons composed of two or more genes. It remains under debate whether the operon organization maintains the stoichiometric expression of the genes within an operon. In this study, we performed a label-free data-in...

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Autores principales: Zhao, Jing, Zhang, Hong, Qin, Bo, Nikolay, Rainer, He, Qing-Yu, Spahn, Christian M. T., Zhang, Gong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6544118/
https://www.ncbi.nlm.nih.gov/pubmed/31178895
http://dx.doi.org/10.3389/fgene.2019.00473
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author Zhao, Jing
Zhang, Hong
Qin, Bo
Nikolay, Rainer
He, Qing-Yu
Spahn, Christian M. T.
Zhang, Gong
author_facet Zhao, Jing
Zhang, Hong
Qin, Bo
Nikolay, Rainer
He, Qing-Yu
Spahn, Christian M. T.
Zhang, Gong
author_sort Zhao, Jing
collection PubMed
description More than half of the protein-coding genes in bacteria are organized in polycistronic operons composed of two or more genes. It remains under debate whether the operon organization maintains the stoichiometric expression of the genes within an operon. In this study, we performed a label-free data-independent acquisition hyper reaction monitoring mass-spectrometry (HRM-MS) experiment to quantify the Escherichia coli proteome in exponential phase and quantified 93.6% of the cytosolic proteins, covering 67.9% and 56.0% of the translating polycistronic operons in BW25113 and MG1655 strains, respectively. We found that the translational regulation contributes largely to the proteome complexity: the shorter operons tend to be more tightly controlled for stoichiometry than longer operons; the operons which mainly code for complexes is more tightly controlled for stoichiometry than the operons which mainly code for metabolic pathways. The gene interval (distance between adjacent genes in one operon) may serve as a regulatory factor for stoichiometry. The catalytic efficiency might be a driving force for differential expression of enzymes encoded in one operon. These results illustrated the multifaceted nature of the operon regulation: the operon unified transcriptional level and gene-specific translational level. This multi-level regulation benefits the host by optimizing the efficiency of the productivity of metabolic pathways and maintenance of different types of protein complexes.
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spelling pubmed-65441182019-06-07 Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification Zhao, Jing Zhang, Hong Qin, Bo Nikolay, Rainer He, Qing-Yu Spahn, Christian M. T. Zhang, Gong Front Genet Genetics More than half of the protein-coding genes in bacteria are organized in polycistronic operons composed of two or more genes. It remains under debate whether the operon organization maintains the stoichiometric expression of the genes within an operon. In this study, we performed a label-free data-independent acquisition hyper reaction monitoring mass-spectrometry (HRM-MS) experiment to quantify the Escherichia coli proteome in exponential phase and quantified 93.6% of the cytosolic proteins, covering 67.9% and 56.0% of the translating polycistronic operons in BW25113 and MG1655 strains, respectively. We found that the translational regulation contributes largely to the proteome complexity: the shorter operons tend to be more tightly controlled for stoichiometry than longer operons; the operons which mainly code for complexes is more tightly controlled for stoichiometry than the operons which mainly code for metabolic pathways. The gene interval (distance between adjacent genes in one operon) may serve as a regulatory factor for stoichiometry. The catalytic efficiency might be a driving force for differential expression of enzymes encoded in one operon. These results illustrated the multifaceted nature of the operon regulation: the operon unified transcriptional level and gene-specific translational level. This multi-level regulation benefits the host by optimizing the efficiency of the productivity of metabolic pathways and maintenance of different types of protein complexes. Frontiers Media S.A. 2019-05-24 /pmc/articles/PMC6544118/ /pubmed/31178895 http://dx.doi.org/10.3389/fgene.2019.00473 Text en Copyright © 2019 Zhao, Zhang, Qin, Nikolay, He, Spahn and Zhang. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Genetics
Zhao, Jing
Zhang, Hong
Qin, Bo
Nikolay, Rainer
He, Qing-Yu
Spahn, Christian M. T.
Zhang, Gong
Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification
title Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification
title_full Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification
title_fullStr Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification
title_full_unstemmed Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification
title_short Multifaceted Stoichiometry Control of Bacterial Operons Revealed by Deep Proteome Quantification
title_sort multifaceted stoichiometry control of bacterial operons revealed by deep proteome quantification
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6544118/
https://www.ncbi.nlm.nih.gov/pubmed/31178895
http://dx.doi.org/10.3389/fgene.2019.00473
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