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Title: 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 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.

Authors:
; ; ; ; ; ; ; ORCiD logo; ; ORCiD logo
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
OSTI Identifier:
1619864
Alternate Identifier(s):
OSTI ID: 1770292
Report Number(s):
PNNL-SA-155824
Journal ID: ISSN 2150-7511; e00957-20; /mbio/11/3/mBio.00957-20.atom
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231; SC0018409; R01AI097157
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 11 Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; rhodobacter; cell division; cell envelope; lipopolysaccharide; peptidoglycan; periplasm; proteobacteria; two-component system

Citation Formats

Lemmer, Kimberly C., Alberge, François, Myers, Kevin S., Dohnalkova, Alice C., Schaub, Ryan E., Lenz, Jonathan D., Imam, Saheed, Dillard, Joseph P., Noguera, Daniel R., and Donohue, Timothy J. The NtrYX Two-Component System Regulates the Bacterial Cell Envelope. United States: N. p., 2020. Web. doi:10.1128/mbio.00957-20.
Lemmer, Kimberly C., Alberge, François, Myers, Kevin S., Dohnalkova, Alice C., Schaub, Ryan E., Lenz, Jonathan D., Imam, Saheed, Dillard, Joseph P., Noguera, Daniel R., & Donohue, Timothy J. The NtrYX Two-Component System Regulates the Bacterial Cell Envelope. United States. doi:https://doi.org/10.1128/mbio.00957-20
Lemmer, Kimberly C., Alberge, François, Myers, Kevin S., Dohnalkova, Alice C., Schaub, Ryan E., Lenz, Jonathan D., Imam, Saheed, Dillard, Joseph P., Noguera, Daniel R., and Donohue, Timothy J. Tue . "The NtrYX Two-Component System Regulates the Bacterial Cell Envelope". United States. doi:https://doi.org/10.1128/mbio.00957-20.
@article{osti_1619864,
title = {The NtrYX Two-Component System Regulates the Bacterial Cell Envelope},
author = {Lemmer, Kimberly C. and Alberge, François and Myers, Kevin S. and Dohnalkova, Alice C. and Schaub, Ryan E. and Lenz, Jonathan D. and Imam, Saheed and Dillard, Joseph P. and Noguera, Daniel R. and Donohue, Timothy J.},
abstractNote = {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.},
doi = {10.1128/mbio.00957-20},
journal = {mBio (Online)},
number = 3,
volume = 11,
place = {United States},
year = {2020},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
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DOI: https://doi.org/10.1128/mbio.00957-20

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