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Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli

Rapid dissemination of the plasmid-born polymyxin resistance gene mcr-1 poses a critical medical challenge. MCR-1 expression is tightly controlled and imposes a fitness cost on the bacteria. We used growth studies and metabolomics to examine growth and metabolic changes within E. coli TOP10 at 8 and...

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Autores principales: Liu, Yi-Yun, Zhu, Yan, Wickremasinghe, Hasini, Bergen, Phillip J., Lu, Jing, Zhu, Xiao-Qing, Zhou, Qiao-Li, Azad, Mohammad, Nang, Sue C., Han, Mei-Ling, Lei, Tao, Li, Jian, Liu, Jian-Hua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7581681/
https://www.ncbi.nlm.nih.gov/pubmed/33162965
http://dx.doi.org/10.3389/fmicb.2020.588658
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author Liu, Yi-Yun
Zhu, Yan
Wickremasinghe, Hasini
Bergen, Phillip J.
Lu, Jing
Zhu, Xiao-Qing
Zhou, Qiao-Li
Azad, Mohammad
Nang, Sue C.
Han, Mei-Ling
Lei, Tao
Li, Jian
Liu, Jian-Hua
author_facet Liu, Yi-Yun
Zhu, Yan
Wickremasinghe, Hasini
Bergen, Phillip J.
Lu, Jing
Zhu, Xiao-Qing
Zhou, Qiao-Li
Azad, Mohammad
Nang, Sue C.
Han, Mei-Ling
Lei, Tao
Li, Jian
Liu, Jian-Hua
author_sort Liu, Yi-Yun
collection PubMed
description Rapid dissemination of the plasmid-born polymyxin resistance gene mcr-1 poses a critical medical challenge. MCR-1 expression is tightly controlled and imposes a fitness cost on the bacteria. We used growth studies and metabolomics to examine growth and metabolic changes within E. coli TOP10 at 8 and 24 h in response to different levels of expression of mcr-1. Induction of mcr-1 greatly increased expression at 8 h and markedly reduced bacterial growth; membrane disruption and cell lysis were evident at this time. At 24 h, the expression of mcr-1 dramatically declined with restored growth and membrane integrity, indicating regulation of mcr-1 expression in bacteria to maintain membrane homeostasis. Intermediates of peptide and lipid biosynthesis were the most commonly affected metabolites when mcr-1 was overexpressed in E. coli. Cell wall biosynthesis was dramatically affected with the accumulation of lipids including fatty acids, glycerophospholipids and lysophosphatidylethanolamines, especially at 8 h. In contrast, levels of intermediate metabolites of peptides, amino sugars, carbohydrates and nucleotide metabolism and secondary metabolites significantly decreased. Moreover, the over-expression of mcr-1 resulted in a prolonged reduction in intermediates associated with pentose phosphate pathway and pantothenate and CoA biosynthesis. These findings indicate that over-expression of mcr-1 results in global metabolic perturbations that mainly involve disruption to the bacterial membrane, pentose phosphate pathway as well as pantothenate and CoA biosynthesis.
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spelling pubmed-75816812020-11-05 Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli Liu, Yi-Yun Zhu, Yan Wickremasinghe, Hasini Bergen, Phillip J. Lu, Jing Zhu, Xiao-Qing Zhou, Qiao-Li Azad, Mohammad Nang, Sue C. Han, Mei-Ling Lei, Tao Li, Jian Liu, Jian-Hua Front Microbiol Microbiology Rapid dissemination of the plasmid-born polymyxin resistance gene mcr-1 poses a critical medical challenge. MCR-1 expression is tightly controlled and imposes a fitness cost on the bacteria. We used growth studies and metabolomics to examine growth and metabolic changes within E. coli TOP10 at 8 and 24 h in response to different levels of expression of mcr-1. Induction of mcr-1 greatly increased expression at 8 h and markedly reduced bacterial growth; membrane disruption and cell lysis were evident at this time. At 24 h, the expression of mcr-1 dramatically declined with restored growth and membrane integrity, indicating regulation of mcr-1 expression in bacteria to maintain membrane homeostasis. Intermediates of peptide and lipid biosynthesis were the most commonly affected metabolites when mcr-1 was overexpressed in E. coli. Cell wall biosynthesis was dramatically affected with the accumulation of lipids including fatty acids, glycerophospholipids and lysophosphatidylethanolamines, especially at 8 h. In contrast, levels of intermediate metabolites of peptides, amino sugars, carbohydrates and nucleotide metabolism and secondary metabolites significantly decreased. Moreover, the over-expression of mcr-1 resulted in a prolonged reduction in intermediates associated with pentose phosphate pathway and pantothenate and CoA biosynthesis. These findings indicate that over-expression of mcr-1 results in global metabolic perturbations that mainly involve disruption to the bacterial membrane, pentose phosphate pathway as well as pantothenate and CoA biosynthesis. Frontiers Media S.A. 2020-10-09 /pmc/articles/PMC7581681/ /pubmed/33162965 http://dx.doi.org/10.3389/fmicb.2020.588658 Text en Copyright © 2020 Liu, Zhu, Wickremasinghe, Bergen, Lu, Zhu, Zhou, Azad, Nang, Han, Lei, Li and Liu. 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 Microbiology
Liu, Yi-Yun
Zhu, Yan
Wickremasinghe, Hasini
Bergen, Phillip J.
Lu, Jing
Zhu, Xiao-Qing
Zhou, Qiao-Li
Azad, Mohammad
Nang, Sue C.
Han, Mei-Ling
Lei, Tao
Li, Jian
Liu, Jian-Hua
Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli
title Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli
title_full Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli
title_fullStr Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli
title_full_unstemmed Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli
title_short Metabolic Perturbations Caused by the Over-Expression of mcr-1 in Escherichia coli
title_sort metabolic perturbations caused by the over-expression of mcr-1 in escherichia coli
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7581681/
https://www.ncbi.nlm.nih.gov/pubmed/33162965
http://dx.doi.org/10.3389/fmicb.2020.588658
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