Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System

ABSTRACT Cell density-dependent regulation of gene expression in Xylella fastidiosa that is crucial to its switching between plant hosts and insect vectors is dependent on RpfF and its production of 2-enoic acids known as diffusible signal factor (DSF). We show that X. fastidiosa produces a particul...

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Autores principales:	Michael Ionescu, Kenji Yokota, Elena Antonova, Angelica Garcia, Ellen Beaulieu, Terry Hayes, Anthony T. Iavarone, Steven E. Lindow
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
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spelling	oai:doaj.org-article:3d1c64ff404f496bb323e2b78b3bf7a62021-11-15T15:50:18ZPromiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System10.1128/mBio.01054-162150-7511https://doaj.org/article/3d1c64ff404f496bb323e2b78b3bf7a62016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01054-16https://doaj.org/toc/2150-7511ABSTRACT Cell density-dependent regulation of gene expression in Xylella fastidiosa that is crucial to its switching between plant hosts and insect vectors is dependent on RpfF and its production of 2-enoic acids known as diffusible signal factor (DSF). We show that X. fastidiosa produces a particularly large variety of similar, relatively long-chain-length 2-enoic acids that are active in modulating gene expression. Both X. fastidiosa itself and a Pantoea agglomerans surrogate host harboring X. fastidiosa RpfF (XfRpfF) is capable of producing a variety of both saturated and unsaturated free fatty acids. However, only 2-cis unsaturated acids were found to be biologically active in X. fastidiosa. X. fastidiosa produces, and is particularly responsive to, a novel DSF species, 2-cis-hexadecanoic acid that we term XfDSF2. It is also responsive to other, even longer 2-enoic acids to which other taxa such as Xanthomonas campestris are unresponsive. The 2-enoic acids that are produced by X. fastidiosa are strongly affected by the cellular growth environment, with XfDSF2 not detected in culture media in which 2-tetradecenoic acid (XfDSF1) had previously been found. X. fastidiosa is responsive to much lower concentrations of XfDSF2 than XfDSF1. Apparently competitive interactions can occur between various saturated and unsaturated fatty acids that block the function of those agonistic 2-enoic fatty acids. By altering the particular 2-enoic acids produced and the relative balance of free enoic and saturated fatty acids, X. fastidiosa might modulate the extent of DSF-mediated quorum sensing. IMPORTANCE X. fastidiosa, having a complicated lifestyle in which it moves and multiplies within plants but also must be vectored by insects, utilizes DSF-based quorum sensing to partition the expression of traits needed for these two processes within different cells in this population based on local cellular density. The finding that it can produce a variety of DSF species in a strongly environmentally context-dependent manner provides insight into how it coordinates the many genes under the control of DSF signaling to successfully associate with its two hosts. Since the new DSF variant XfDSF2 described here is much more active than the previously recognized DSF species, it should contribute to plant disease control, given that the susceptibility of plants can be greatly reduced by artificially elevating the levels of DSF in plants, creating “pathogen confusion,” resulting in lower virulence.Michael IonescuKenji YokotaElena AntonovaAngelica GarciaEllen BeaulieuTerry HayesAnthony T. IavaroneSteven E. LindowAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Michael Ionescu Kenji Yokota Elena Antonova Angelica Garcia Ellen Beaulieu Terry Hayes Anthony T. Iavarone Steven E. Lindow Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System
description	ABSTRACT Cell density-dependent regulation of gene expression in Xylella fastidiosa that is crucial to its switching between plant hosts and insect vectors is dependent on RpfF and its production of 2-enoic acids known as diffusible signal factor (DSF). We show that X. fastidiosa produces a particularly large variety of similar, relatively long-chain-length 2-enoic acids that are active in modulating gene expression. Both X. fastidiosa itself and a Pantoea agglomerans surrogate host harboring X. fastidiosa RpfF (XfRpfF) is capable of producing a variety of both saturated and unsaturated free fatty acids. However, only 2-cis unsaturated acids were found to be biologically active in X. fastidiosa. X. fastidiosa produces, and is particularly responsive to, a novel DSF species, 2-cis-hexadecanoic acid that we term XfDSF2. It is also responsive to other, even longer 2-enoic acids to which other taxa such as Xanthomonas campestris are unresponsive. The 2-enoic acids that are produced by X. fastidiosa are strongly affected by the cellular growth environment, with XfDSF2 not detected in culture media in which 2-tetradecenoic acid (XfDSF1) had previously been found. X. fastidiosa is responsive to much lower concentrations of XfDSF2 than XfDSF1. Apparently competitive interactions can occur between various saturated and unsaturated fatty acids that block the function of those agonistic 2-enoic fatty acids. By altering the particular 2-enoic acids produced and the relative balance of free enoic and saturated fatty acids, X. fastidiosa might modulate the extent of DSF-mediated quorum sensing. IMPORTANCE X. fastidiosa, having a complicated lifestyle in which it moves and multiplies within plants but also must be vectored by insects, utilizes DSF-based quorum sensing to partition the expression of traits needed for these two processes within different cells in this population based on local cellular density. The finding that it can produce a variety of DSF species in a strongly environmentally context-dependent manner provides insight into how it coordinates the many genes under the control of DSF signaling to successfully associate with its two hosts. Since the new DSF variant XfDSF2 described here is much more active than the previously recognized DSF species, it should contribute to plant disease control, given that the susceptibility of plants can be greatly reduced by artificially elevating the levels of DSF in plants, creating “pathogen confusion,” resulting in lower virulence.
format	article
author	Michael Ionescu Kenji Yokota Elena Antonova Angelica Garcia Ellen Beaulieu Terry Hayes Anthony T. Iavarone Steven E. Lindow
author_facet	Michael Ionescu Kenji Yokota Elena Antonova Angelica Garcia Ellen Beaulieu Terry Hayes Anthony T. Iavarone Steven E. Lindow
author_sort	Michael Ionescu
title	Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System
title_short	Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System
title_full	Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System
title_fullStr	Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System
title_full_unstemmed	Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System
title_sort	promiscuous diffusible signal factor production and responsiveness of the <named-content content-type="genus-species">xylella fastidiosa</named-content> rpf system
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/3d1c64ff404f496bb323e2b78b3bf7a6
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Promiscuous Diffusible Signal Factor Production and Responsiveness of the <named-content content-type="genus-species">Xylella fastidiosa</named-content> Rpf System

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