The NtrYX Two-Component System Regulates the Bacterial Cell Envelope

ABSTRACT Activity of the NtrYX two-component system has been associated with important processes in diverse bacteria, ranging from symbiosis to nitrogen and energy metabolism. In the facultative alphaproteobacterium Rhodobacter sphaeroides, loss of the two-component system NtrYX results in increased...

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Autores principales:	Kimberly C. Lemmer, François Alberge, Kevin S. Myers, Alice C. Dohnalkova, Ryan E. Schaub, Jonathan D. Lenz, Saheed Imam, Joseph P. Dillard, Daniel R. Noguera, Timothy J. Donohue
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Rhodobacter cell division cell envelope lipopolysaccharide peptidoglycan periplasm Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5ed8aa6fd54840b8a06ab1cadfe5e933
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spelling	oai:doaj.org-article:5ed8aa6fd54840b8a06ab1cadfe5e9332021-11-15T15:56:47ZThe NtrYX Two-Component System Regulates the Bacterial Cell Envelope10.1128/mBio.00957-202150-7511https://doaj.org/article/5ed8aa6fd54840b8a06ab1cadfe5e9332020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00957-20https://doaj.org/toc/2150-7511ABSTRACT Activity of the NtrYX two-component system has been associated with important processes in diverse bacteria, ranging from symbiosis to nitrogen and energy metabolism. In the facultative alphaproteobacterium Rhodobacter sphaeroides, loss of the two-component system NtrYX results in increased lipid production and sensitivity to some known cell envelope-active compounds. In this study, we show that NtrYX directly controls multiple properties of the cell envelope. We find that the response regulator NtrX binds upstream of cell envelope genes, including those involved in peptidoglycan biosynthesis and modification and in cell division. We show that loss of NtrYX impacts the cellular levels of peptidoglycan precursors and lipopolysaccharide and alters cell envelope structure, increasing cell length and the thickness of the periplasm. Cell envelope function is also disrupted in the absence of NtrYX, resulting in increased outer membrane permeability. Based on the properties of R. sphaeroides cells lacking NtrYX and the target genes under direct control of this two-component system, we propose that NtrYX plays a previously undescribed, and potentially conserved, role in the assembly, structure, and function of the cell envelope in a variety of bacteria. IMPORTANCE The bacterial cell envelope provides many important functions. It protects cells from harsh environments, serves as a selective permeability barrier, houses bioenergetic functions, defines sensitivity to antibacterial agents, and plays a crucial role in biofilm formation, symbiosis, and virulence. Despite the important roles of this cellular compartment, we lack a detailed understanding of the biosynthesis and remodeling of the cell envelope. Here, we report that the R. sphaeroides two-component signaling system NtrYX is a previously undescribed regulator of cell envelope processes, providing evidence that it is directly involved in controlling transcription of genes involved in cell envelope assembly, structure, and function in this and possibly other bacteria. Thus, our data report on a newly discovered process used by bacteria to assemble and remodel the cell envelope.Kimberly C. LemmerFrançois AlbergeKevin S. MyersAlice C. DohnalkovaRyan E. SchaubJonathan D. LenzSaheed ImamJoseph P. DillardDaniel R. NogueraTimothy J. DonohueAmerican Society for MicrobiologyarticleRhodobactercell divisioncell envelopelipopolysaccharidepeptidoglycanperiplasmMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Rhodobacter cell division cell envelope lipopolysaccharide peptidoglycan periplasm Microbiology QR1-502
spellingShingle	Rhodobacter cell division cell envelope lipopolysaccharide peptidoglycan periplasm Microbiology QR1-502 Kimberly C. Lemmer François Alberge Kevin S. Myers Alice C. Dohnalkova Ryan E. Schaub Jonathan D. Lenz Saheed Imam Joseph P. Dillard Daniel R. Noguera Timothy J. Donohue The NtrYX Two-Component System Regulates the Bacterial Cell Envelope
description	ABSTRACT Activity of the NtrYX two-component system has been associated with important processes in diverse bacteria, ranging from symbiosis to nitrogen and energy metabolism. In the facultative alphaproteobacterium Rhodobacter sphaeroides, loss of the two-component system NtrYX results in increased lipid production and sensitivity to some known cell envelope-active compounds. In this study, we show that NtrYX directly controls multiple properties of the cell envelope. We find that the response regulator NtrX binds upstream of cell envelope genes, including those involved in peptidoglycan biosynthesis and modification and in cell division. We show that loss of NtrYX impacts the cellular levels of peptidoglycan precursors and lipopolysaccharide and alters cell envelope structure, increasing cell length and the thickness of the periplasm. Cell envelope function is also disrupted in the absence of NtrYX, resulting in increased outer membrane permeability. Based on the properties of R. sphaeroides cells lacking NtrYX and the target genes under direct control of this two-component system, we propose that NtrYX plays a previously undescribed, and potentially conserved, role in the assembly, structure, and function of the cell envelope in a variety of bacteria. IMPORTANCE The bacterial cell envelope provides many important functions. It protects cells from harsh environments, serves as a selective permeability barrier, houses bioenergetic functions, defines sensitivity to antibacterial agents, and plays a crucial role in biofilm formation, symbiosis, and virulence. Despite the important roles of this cellular compartment, we lack a detailed understanding of the biosynthesis and remodeling of the cell envelope. Here, we report that the R. sphaeroides two-component signaling system NtrYX is a previously undescribed regulator of cell envelope processes, providing evidence that it is directly involved in controlling transcription of genes involved in cell envelope assembly, structure, and function in this and possibly other bacteria. Thus, our data report on a newly discovered process used by bacteria to assemble and remodel the cell envelope.
format	article
author	Kimberly C. Lemmer François Alberge Kevin S. Myers Alice C. Dohnalkova Ryan E. Schaub Jonathan D. Lenz Saheed Imam Joseph P. Dillard Daniel R. Noguera Timothy J. Donohue
author_facet	Kimberly C. Lemmer François Alberge Kevin S. Myers Alice C. Dohnalkova Ryan E. Schaub Jonathan D. Lenz Saheed Imam Joseph P. Dillard Daniel R. Noguera Timothy J. Donohue
author_sort	Kimberly C. Lemmer
title	The NtrYX Two-Component System Regulates the Bacterial Cell Envelope
title_short	The NtrYX Two-Component System Regulates the Bacterial Cell Envelope
title_full	The NtrYX Two-Component System Regulates the Bacterial Cell Envelope
title_fullStr	The NtrYX Two-Component System Regulates the Bacterial Cell Envelope
title_full_unstemmed	The NtrYX Two-Component System Regulates the Bacterial Cell Envelope
title_sort	ntryx two-component system regulates the bacterial cell envelope
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/5ed8aa6fd54840b8a06ab1cadfe5e933
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The NtrYX Two-Component System Regulates the Bacterial Cell Envelope

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