The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells

ABSTRACT The bacterial cell poles are emerging as subdomains where many cellular activities take place, but the mechanisms for polar localization are just beginning to unravel. The general phosphotransferase system (PTS) proteins, enzyme I (EI) and HPr, which control preferential use of carbon sourc...

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Autores principales:	Sutharsan Govindarajan, Yair Elisha, Keren Nevo-Dinur, Orna Amster-Choder
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2d25896dcb7a45729726d096709f66a5
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spelling	oai:doaj.org-article:2d25896dcb7a45729726d096709f66a52021-11-15T15:42:48ZThe General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells10.1128/mBio.00443-132150-7511https://doaj.org/article/2d25896dcb7a45729726d096709f66a52013-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00443-13https://doaj.org/toc/2150-7511ABSTRACT The bacterial cell poles are emerging as subdomains where many cellular activities take place, but the mechanisms for polar localization are just beginning to unravel. The general phosphotransferase system (PTS) proteins, enzyme I (EI) and HPr, which control preferential use of carbon sources in bacteria, were recently shown to localize near the Escherichia coli cell poles. Here, we show that EI localization does not depend on known polar constituents, such as anionic lipids or the chemotaxis receptors, and on the cell division machinery, nor can it be explained by nucleoid occlusion or localized translation. Detection of the general PTS proteins at the budding sites of endocytotic-like membrane invaginations in spherical cells and their colocalization with the negative curvature sensor protein DivIVA suggest that geometric cues underlie localization of the PTS system. Notably, the kinetics of glucose uptake by spherical and rod-shaped E. coli cells are comparable, implying that negatively curved “pole-like” sites support not only the localization but also the proper functioning of the PTS system in cells with different shapes. Consistent with the curvature-mediated localization model, we observed the EI protein from Bacillus subtilis at strongly curved sites in both B. subtilis and E. coli. Taken together, we propose that changes in cell architecture correlate with dynamic survival strategies that localize central metabolic systems like the PTS to subcellular domains where they remain active, thus maintaining cell viability and metabolic alertness. IMPORTANCE Despite their tiny size and the scarcity of membrane-bounded organelles, bacteria are capable of sorting macromolecules to distinct subcellular domains, thus optimizing functionality of vital processes. Understanding the cues that organize bacterial cells should provide novel insights into the complex organization of higher organisms. Previously, we have shown that the general proteins of the phosphotransferase system (PTS) signaling system, which governs utilization of carbon sources in bacteria, localize to the poles of Escherichia coli cells. Here, we show that geometric cues, i.e., strong negative membrane curvature, mediate positioning of the PTS proteins. Furthermore, localization to negatively curved regions seems to support the PTS functionality.Sutharsan GovindarajanYair ElishaKeren Nevo-DinurOrna Amster-ChoderAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 5 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Sutharsan Govindarajan Yair Elisha Keren Nevo-Dinur Orna Amster-Choder The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells
description	ABSTRACT The bacterial cell poles are emerging as subdomains where many cellular activities take place, but the mechanisms for polar localization are just beginning to unravel. The general phosphotransferase system (PTS) proteins, enzyme I (EI) and HPr, which control preferential use of carbon sources in bacteria, were recently shown to localize near the Escherichia coli cell poles. Here, we show that EI localization does not depend on known polar constituents, such as anionic lipids or the chemotaxis receptors, and on the cell division machinery, nor can it be explained by nucleoid occlusion or localized translation. Detection of the general PTS proteins at the budding sites of endocytotic-like membrane invaginations in spherical cells and their colocalization with the negative curvature sensor protein DivIVA suggest that geometric cues underlie localization of the PTS system. Notably, the kinetics of glucose uptake by spherical and rod-shaped E. coli cells are comparable, implying that negatively curved “pole-like” sites support not only the localization but also the proper functioning of the PTS system in cells with different shapes. Consistent with the curvature-mediated localization model, we observed the EI protein from Bacillus subtilis at strongly curved sites in both B. subtilis and E. coli. Taken together, we propose that changes in cell architecture correlate with dynamic survival strategies that localize central metabolic systems like the PTS to subcellular domains where they remain active, thus maintaining cell viability and metabolic alertness. IMPORTANCE Despite their tiny size and the scarcity of membrane-bounded organelles, bacteria are capable of sorting macromolecules to distinct subcellular domains, thus optimizing functionality of vital processes. Understanding the cues that organize bacterial cells should provide novel insights into the complex organization of higher organisms. Previously, we have shown that the general proteins of the phosphotransferase system (PTS) signaling system, which governs utilization of carbon sources in bacteria, localize to the poles of Escherichia coli cells. Here, we show that geometric cues, i.e., strong negative membrane curvature, mediate positioning of the PTS proteins. Furthermore, localization to negatively curved regions seems to support the PTS functionality.
format	article
author	Sutharsan Govindarajan Yair Elisha Keren Nevo-Dinur Orna Amster-Choder
author_facet	Sutharsan Govindarajan Yair Elisha Keren Nevo-Dinur Orna Amster-Choder
author_sort	Sutharsan Govindarajan
title	The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells
title_short	The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells
title_full	The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells
title_fullStr	The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells
title_full_unstemmed	The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells
title_sort	general phosphotransferase system proteins localize to sites of strong negative curvature in bacterial cells
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/2d25896dcb7a45729726d096709f66a5
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The General Phosphotransferase System Proteins Localize to Sites of Strong Negative Curvature in Bacterial Cells

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