Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria

ABSTRACT Various toxic compounds disrupt bacterial physiology. While bacteria harbor defense mechanisms to mitigate the toxicity, these mechanisms are often coupled to the physiological state of the cells and become ineffective when the physiology is severely disrupted. Here, we characterized such f...

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Autores principales:	Dai Le, Ekaterina Krasnopeeva, Faris Sinjab, Teuta Pilizota, Minsu Kim
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	bacterial physiology single-cell microscopy cell-to-cell heterogeneity efflux pumps proton motive force protonophore Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ff6cfaa9f02e44d3a30ae4d083ae06a8
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spelling	oai:doaj.org-article:ff6cfaa9f02e44d3a30ae4d083ae06a82021-11-10T18:37:50ZActive Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria10.1128/mBio.00676-212150-7511https://doaj.org/article/ff6cfaa9f02e44d3a30ae4d083ae06a82021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00676-21https://doaj.org/toc/2150-7511ABSTRACT Various toxic compounds disrupt bacterial physiology. While bacteria harbor defense mechanisms to mitigate the toxicity, these mechanisms are often coupled to the physiological state of the cells and become ineffective when the physiology is severely disrupted. Here, we characterized such feedback by exposing Escherichia coli to protonophores. Protonophores dissipate the proton motive force (PMF), a fundamental force that drives physiological functions. We found that E. coli cells responded to protonophores heterogeneously, resulting in bimodal distributions of cell growth, substrate transport, and motility. Furthermore, we showed that this heterogeneous response required active efflux systems. The analysis of underlying interactions indicated the heterogeneous response results from efflux-mediated positive feedback between PMF and protonophores’ action. Our studies have broad implications for bacterial adaptation to stress, including antibiotics. IMPORTANCE An electrochemical proton gradient across the cytoplasmic membrane, alternatively known as proton motive force, energizes vital cellular processes in bacteria, including ATP synthesis, nutrient uptake, and cell division. Therefore, a wide range of organisms produce the agents that collapse the proton motive force, protonophores, to gain a competitive advantage. Studies have shown that protonophores have significant effects on microbial competition, host-pathogen interaction, and antibiotic action and resistance. Furthermore, protonophores are extensively used in various laboratory studies to perturb bacterial physiology. Here, we have characterized cell growth, substrate transport, and motility of Escherichia coli cells exposed to protonophores. Our findings demonstrate heterogeneous effects of protonophores on cell physiology and the underlying mechanism.Dai LeEkaterina KrasnopeevaFaris SinjabTeuta PilizotaMinsu KimAmerican Society for Microbiologyarticlebacterial physiologysingle-cell microscopycell-to-cell heterogeneityefflux pumpsproton motive forceprotonophoreMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacterial physiology single-cell microscopy cell-to-cell heterogeneity efflux pumps proton motive force protonophore Microbiology QR1-502
spellingShingle	bacterial physiology single-cell microscopy cell-to-cell heterogeneity efflux pumps proton motive force protonophore Microbiology QR1-502 Dai Le Ekaterina Krasnopeeva Faris Sinjab Teuta Pilizota Minsu Kim Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria
description	ABSTRACT Various toxic compounds disrupt bacterial physiology. While bacteria harbor defense mechanisms to mitigate the toxicity, these mechanisms are often coupled to the physiological state of the cells and become ineffective when the physiology is severely disrupted. Here, we characterized such feedback by exposing Escherichia coli to protonophores. Protonophores dissipate the proton motive force (PMF), a fundamental force that drives physiological functions. We found that E. coli cells responded to protonophores heterogeneously, resulting in bimodal distributions of cell growth, substrate transport, and motility. Furthermore, we showed that this heterogeneous response required active efflux systems. The analysis of underlying interactions indicated the heterogeneous response results from efflux-mediated positive feedback between PMF and protonophores’ action. Our studies have broad implications for bacterial adaptation to stress, including antibiotics. IMPORTANCE An electrochemical proton gradient across the cytoplasmic membrane, alternatively known as proton motive force, energizes vital cellular processes in bacteria, including ATP synthesis, nutrient uptake, and cell division. Therefore, a wide range of organisms produce the agents that collapse the proton motive force, protonophores, to gain a competitive advantage. Studies have shown that protonophores have significant effects on microbial competition, host-pathogen interaction, and antibiotic action and resistance. Furthermore, protonophores are extensively used in various laboratory studies to perturb bacterial physiology. Here, we have characterized cell growth, substrate transport, and motility of Escherichia coli cells exposed to protonophores. Our findings demonstrate heterogeneous effects of protonophores on cell physiology and the underlying mechanism.
format	article
author	Dai Le Ekaterina Krasnopeeva Faris Sinjab Teuta Pilizota Minsu Kim
author_facet	Dai Le Ekaterina Krasnopeeva Faris Sinjab Teuta Pilizota Minsu Kim
author_sort	Dai Le
title	Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria
title_short	Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria
title_full	Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria
title_fullStr	Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria
title_full_unstemmed	Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria
title_sort	active efflux leads to heterogeneous dissipation of proton motive force by protonophores in bacteria
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/ff6cfaa9f02e44d3a30ae4d083ae06a8
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Active Efflux Leads to Heterogeneous Dissipation of Proton Motive Force by Protonophores in Bacteria

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