The gatekeeper of Yersinia type III secretion is under RNA thermometer control.

Many bacterial pathogens use a type III secretion system (T3SS) as molecular syringe to inject effector proteins into the host cell. In the foodborne pathogen Yersinia pseudotuberculosis, delivery of the secreted effector protein cocktail through the T3SS depends on YopN, a molecular gatekeeper that...

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Autores principales:	Stephan Pienkoß, Soheila Javadi, Paweena Chaoprasid, Thomas Nolte, Christian Twittenhoff, Petra Dersch, Franz Narberhaus
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/cbdf07183a714185b4c5eebf5da3cfb2
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spelling	oai:doaj.org-article:cbdf07183a714185b4c5eebf5da3cfb22021-12-02T19:59:57ZThe gatekeeper of Yersinia type III secretion is under RNA thermometer control.1553-73661553-737410.1371/journal.ppat.1009650https://doaj.org/article/cbdf07183a714185b4c5eebf5da3cfb22021-11-01T00:00:00Zhttps://doi.org/10.1371/journal.ppat.1009650https://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Many bacterial pathogens use a type III secretion system (T3SS) as molecular syringe to inject effector proteins into the host cell. In the foodborne pathogen Yersinia pseudotuberculosis, delivery of the secreted effector protein cocktail through the T3SS depends on YopN, a molecular gatekeeper that controls access to the secretion channel from the bacterial cytoplasm. Here, we show that several checkpoints adjust yopN expression to virulence conditions. A dominant cue is the host body temperature. A temperature of 37°C is known to induce the RNA thermometer (RNAT)-dependent synthesis of LcrF, a transcription factor that activates expression of the entire T3SS regulon. Here, we uncovered a second layer of temperature control. We show that another RNAT silences translation of the yopN mRNA at low environmental temperatures. The long and short 5'-untranslated region of both cellular yopN isoforms fold into a similar secondary structure that blocks ribosome binding. The hairpin structure with an internal loop melts at 37°C and thereby permits formation of the translation initiation complex as shown by mutational analysis, in vitro structure probing and toeprinting methods. Importantly, we demonstrate the physiological relevance of the RNAT in the faithful control of type III secretion by using a point-mutated thermostable RNAT variant with a trapped SD sequence. Abrogated YopN production in this strain led to unrestricted effector protein secretion into the medium, bacterial growth arrest and delayed translocation into eukaryotic host cells. Cumulatively, our results show that substrate delivery by the Yersinia T3SS is under hierarchical surveillance of two RNATs.Stephan PienkoßSoheila JavadiPaweena ChaoprasidThomas NolteChristian TwittenhoffPetra DerschFranz NarberhausPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 17, Iss 11, p e1009650 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Stephan Pienkoß Soheila Javadi Paweena Chaoprasid Thomas Nolte Christian Twittenhoff Petra Dersch Franz Narberhaus The gatekeeper of Yersinia type III secretion is under RNA thermometer control.
description	Many bacterial pathogens use a type III secretion system (T3SS) as molecular syringe to inject effector proteins into the host cell. In the foodborne pathogen Yersinia pseudotuberculosis, delivery of the secreted effector protein cocktail through the T3SS depends on YopN, a molecular gatekeeper that controls access to the secretion channel from the bacterial cytoplasm. Here, we show that several checkpoints adjust yopN expression to virulence conditions. A dominant cue is the host body temperature. A temperature of 37°C is known to induce the RNA thermometer (RNAT)-dependent synthesis of LcrF, a transcription factor that activates expression of the entire T3SS regulon. Here, we uncovered a second layer of temperature control. We show that another RNAT silences translation of the yopN mRNA at low environmental temperatures. The long and short 5'-untranslated region of both cellular yopN isoforms fold into a similar secondary structure that blocks ribosome binding. The hairpin structure with an internal loop melts at 37°C and thereby permits formation of the translation initiation complex as shown by mutational analysis, in vitro structure probing and toeprinting methods. Importantly, we demonstrate the physiological relevance of the RNAT in the faithful control of type III secretion by using a point-mutated thermostable RNAT variant with a trapped SD sequence. Abrogated YopN production in this strain led to unrestricted effector protein secretion into the medium, bacterial growth arrest and delayed translocation into eukaryotic host cells. Cumulatively, our results show that substrate delivery by the Yersinia T3SS is under hierarchical surveillance of two RNATs.
format	article
author	Stephan Pienkoß Soheila Javadi Paweena Chaoprasid Thomas Nolte Christian Twittenhoff Petra Dersch Franz Narberhaus
author_facet	Stephan Pienkoß Soheila Javadi Paweena Chaoprasid Thomas Nolte Christian Twittenhoff Petra Dersch Franz Narberhaus
author_sort	Stephan Pienkoß
title	The gatekeeper of Yersinia type III secretion is under RNA thermometer control.
title_short	The gatekeeper of Yersinia type III secretion is under RNA thermometer control.
title_full	The gatekeeper of Yersinia type III secretion is under RNA thermometer control.
title_fullStr	The gatekeeper of Yersinia type III secretion is under RNA thermometer control.
title_full_unstemmed	The gatekeeper of Yersinia type III secretion is under RNA thermometer control.
title_sort	gatekeeper of yersinia type iii secretion is under rna thermometer control.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/cbdf07183a714185b4c5eebf5da3cfb2
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The gatekeeper of Yersinia type III secretion is under RNA thermometer control.

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