Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response

ABSTRACT Many proteobacteria utilize acyl-homoserine lactone quorum-sensing signals. At low population densities, cells produce a basal level of signal, and when sufficient signal has accumulated in the surrounding environment, it binds to its receptor, and quorum-sensing-dependent genes can be acti...

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Autores principales:	Rebecca L. Scholz, E. Peter Greenberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	bacterial communication cell-cell signaling transcriptional activation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/00cdcc809da849fc9e66f01b0286a391
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spelling	oai:doaj.org-article:00cdcc809da849fc9e66f01b0286a3912021-11-15T15:51:43ZPositive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response10.1128/mBio.01079-172150-7511https://doaj.org/article/00cdcc809da849fc9e66f01b0286a3912017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01079-17https://doaj.org/toc/2150-7511ABSTRACT Many proteobacteria utilize acyl-homoserine lactone quorum-sensing signals. At low population densities, cells produce a basal level of signal, and when sufficient signal has accumulated in the surrounding environment, it binds to its receptor, and quorum-sensing-dependent genes can be activated. A common characteristic of acyl-homoserine lactone quorum sensing is that signal production is positively autoregulated. We have examined the role of positive signal autoregulation in Pseudomonas aeruginosa. We compared population responses and individual cell responses in populations of wild-type P. aeruginosa to responses in a strain with the signal synthase gene controlled by an arabinose-inducible promoter so that signal was produced at a constant rate per cell regardless of cell population density. At a population level, responses of the wild type and the engineered strain were indistinguishable, but the responses of individual cells in a population of the wild type showed greater synchrony than the responses of the engineered strain. Although sufficient signal is required to activate expression of quorum-sensing-regulated genes, it is not sufficient for activation of certain genes, the late genes, and their expression is delayed until other conditions are met. We found that late gene responses were reduced in the engineered strain. We conclude that positive signal autoregulation is not a required element in acyl-homoserine lactone quorum sensing, but it functions to enhance synchrony of the responses of individuals in a population. Synchrony might be advantageous in some situations, whereas a less coordinated quorum-sensing response might allow bet hedging and be advantageous in other situations. IMPORTANCE There are many quorum-sensing systems that involve a transcriptional activator, which responds to an acyl-homoserine lactone signal. In all of the examples studied, the gene coding for signal production is positively autoregulated by the signal, and it has even been described as essential for a quorum-sensing response. We have used the opportunistic pathogen Pseudomonas aeruginosa as a model to show that positive autoregulation is not required for a robust quorum-sensing response. We also show that positive autoregulation of signal production enhances the synchrony of the response. This information enhances our general understanding of the biological significance of how acyl-homoserine lactone quorum-sensing circuits are arranged.Rebecca L. ScholzE. Peter GreenbergAmerican Society for Microbiologyarticlebacterial communicationcell-cell signalingtranscriptional activationMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacterial communication cell-cell signaling transcriptional activation Microbiology QR1-502
spellingShingle	bacterial communication cell-cell signaling transcriptional activation Microbiology QR1-502 Rebecca L. Scholz E. Peter Greenberg Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response
description	ABSTRACT Many proteobacteria utilize acyl-homoserine lactone quorum-sensing signals. At low population densities, cells produce a basal level of signal, and when sufficient signal has accumulated in the surrounding environment, it binds to its receptor, and quorum-sensing-dependent genes can be activated. A common characteristic of acyl-homoserine lactone quorum sensing is that signal production is positively autoregulated. We have examined the role of positive signal autoregulation in Pseudomonas aeruginosa. We compared population responses and individual cell responses in populations of wild-type P. aeruginosa to responses in a strain with the signal synthase gene controlled by an arabinose-inducible promoter so that signal was produced at a constant rate per cell regardless of cell population density. At a population level, responses of the wild type and the engineered strain were indistinguishable, but the responses of individual cells in a population of the wild type showed greater synchrony than the responses of the engineered strain. Although sufficient signal is required to activate expression of quorum-sensing-regulated genes, it is not sufficient for activation of certain genes, the late genes, and their expression is delayed until other conditions are met. We found that late gene responses were reduced in the engineered strain. We conclude that positive signal autoregulation is not a required element in acyl-homoserine lactone quorum sensing, but it functions to enhance synchrony of the responses of individuals in a population. Synchrony might be advantageous in some situations, whereas a less coordinated quorum-sensing response might allow bet hedging and be advantageous in other situations. IMPORTANCE There are many quorum-sensing systems that involve a transcriptional activator, which responds to an acyl-homoserine lactone signal. In all of the examples studied, the gene coding for signal production is positively autoregulated by the signal, and it has even been described as essential for a quorum-sensing response. We have used the opportunistic pathogen Pseudomonas aeruginosa as a model to show that positive autoregulation is not required for a robust quorum-sensing response. We also show that positive autoregulation of signal production enhances the synchrony of the response. This information enhances our general understanding of the biological significance of how acyl-homoserine lactone quorum-sensing circuits are arranged.
format	article
author	Rebecca L. Scholz E. Peter Greenberg
author_facet	Rebecca L. Scholz E. Peter Greenberg
author_sort	Rebecca L. Scholz
title	Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response
title_short	Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response
title_full	Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response
title_fullStr	Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response
title_full_unstemmed	Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response
title_sort	positive autoregulation of an acyl-homoserine lactone quorum-sensing circuit synchronizes the population response
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/00cdcc809da849fc9e66f01b0286a391
work_keys_str_mv	AT rebeccalscholz positiveautoregulationofanacylhomoserinelactonequorumsensingcircuitsynchronizesthepopulationresponse AT epetergreenberg positiveautoregulationofanacylhomoserinelactonequorumsensingcircuitsynchronizesthepopulationresponse
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Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response

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