Cargando…
The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis
Bacterial two-component systems (TCSs) often function through the detection of an extracytoplasmic stimulus and the transduction of a signal by a transmembrane sensory histidine kinase. This kinase then initiates a series of reversible phosphorylation modifications to regulate the activity of a cogn...
Autores principales: | , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9275681/ https://www.ncbi.nlm.nih.gov/pubmed/35767559 http://dx.doi.org/10.1371/journal.pgen.1010270 |
_version_ | 1784745540155604992 |
---|---|
author | Lakey, Bryan D. Myers, Kevin S. Alberge, François Mettert, Erin L. Kiley, Patricia J. Noguera, Daniel R. Donohue, Timothy J. |
author_facet | Lakey, Bryan D. Myers, Kevin S. Alberge, François Mettert, Erin L. Kiley, Patricia J. Noguera, Daniel R. Donohue, Timothy J. |
author_sort | Lakey, Bryan D. |
collection | PubMed |
description | Bacterial two-component systems (TCSs) often function through the detection of an extracytoplasmic stimulus and the transduction of a signal by a transmembrane sensory histidine kinase. This kinase then initiates a series of reversible phosphorylation modifications to regulate the activity of a cognate, cytoplasmic response regulator as a transcription factor. Several TCSs have been implicated in the regulation of cell cycle dynamics, cell envelope integrity, or cell wall development in Escherichia coli and other well-studied Gram-negative model organisms. However, many α-proteobacteria lack homologs to these regulators, so an understanding of how α-proteobacteria orchestrate extracytoplasmic events is lacking. In this work we identify an essential TCS, CenKR (Cell envelope Kinase and Regulator), in the α-proteobacterium Rhodobacter sphaeroides and show that modulation of its activity results in major morphological changes. Using genetic and biochemical approaches, we dissect the requirements for the phosphotransfer event between CenK and CenR, use this information to manipulate the activity of this TCS in vivo, and identify genes that are directly and indirectly controlled by CenKR in Rb. sphaeroides. Combining ChIP-seq and RNA-seq, we show that the CenKR TCS plays a direct role in maintenance of the cell envelope, regulates the expression of subunits of the Tol-Pal outer membrane division complex, and indirectly modulates the expression of peptidoglycan biosynthetic genes. CenKR represents the first TCS reported to directly control the expression of Tol-Pal machinery genes in Gram-negative bacteria, and we predict that homologs of this TCS serve a similar function in other closely related organisms. We propose that Rb. sphaeroides genes of unknown function that are directly regulated by CenKR play unknown roles in cell envelope biosynthesis, assembly, and/or remodeling in this and other α-proteobacteria. |
format | Online Article Text |
id | pubmed-9275681 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-92756812022-07-13 The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis Lakey, Bryan D. Myers, Kevin S. Alberge, François Mettert, Erin L. Kiley, Patricia J. Noguera, Daniel R. Donohue, Timothy J. PLoS Genet Research Article Bacterial two-component systems (TCSs) often function through the detection of an extracytoplasmic stimulus and the transduction of a signal by a transmembrane sensory histidine kinase. This kinase then initiates a series of reversible phosphorylation modifications to regulate the activity of a cognate, cytoplasmic response regulator as a transcription factor. Several TCSs have been implicated in the regulation of cell cycle dynamics, cell envelope integrity, or cell wall development in Escherichia coli and other well-studied Gram-negative model organisms. However, many α-proteobacteria lack homologs to these regulators, so an understanding of how α-proteobacteria orchestrate extracytoplasmic events is lacking. In this work we identify an essential TCS, CenKR (Cell envelope Kinase and Regulator), in the α-proteobacterium Rhodobacter sphaeroides and show that modulation of its activity results in major morphological changes. Using genetic and biochemical approaches, we dissect the requirements for the phosphotransfer event between CenK and CenR, use this information to manipulate the activity of this TCS in vivo, and identify genes that are directly and indirectly controlled by CenKR in Rb. sphaeroides. Combining ChIP-seq and RNA-seq, we show that the CenKR TCS plays a direct role in maintenance of the cell envelope, regulates the expression of subunits of the Tol-Pal outer membrane division complex, and indirectly modulates the expression of peptidoglycan biosynthetic genes. CenKR represents the first TCS reported to directly control the expression of Tol-Pal machinery genes in Gram-negative bacteria, and we predict that homologs of this TCS serve a similar function in other closely related organisms. We propose that Rb. sphaeroides genes of unknown function that are directly regulated by CenKR play unknown roles in cell envelope biosynthesis, assembly, and/or remodeling in this and other α-proteobacteria. Public Library of Science 2022-06-29 /pmc/articles/PMC9275681/ /pubmed/35767559 http://dx.doi.org/10.1371/journal.pgen.1010270 Text en © 2022 Lakey et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Lakey, Bryan D. Myers, Kevin S. Alberge, François Mettert, Erin L. Kiley, Patricia J. Noguera, Daniel R. Donohue, Timothy J. The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis |
title | The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis |
title_full | The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis |
title_fullStr | The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis |
title_full_unstemmed | The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis |
title_short | The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis |
title_sort | essential rhodobacter sphaeroides cenkr two-component system regulates cell division and envelope biosynthesis |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9275681/ https://www.ncbi.nlm.nih.gov/pubmed/35767559 http://dx.doi.org/10.1371/journal.pgen.1010270 |
work_keys_str_mv | AT lakeybryand theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT myerskevins theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT albergefrancois theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT metterterinl theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT kileypatriciaj theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT nogueradanielr theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT donohuetimothyj theessentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT lakeybryand essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT myerskevins essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT albergefrancois essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT metterterinl essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT kileypatriciaj essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT nogueradanielr essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis AT donohuetimothyj essentialrhodobactersphaeroidescenkrtwocomponentsystemregulatescelldivisionandenvelopebiosynthesis |