The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440

ABSTRACT In Pseudomonas putida KT2440, two pyrroloquinoline quinone-dependent ethanol dehydrogenases (PQQ-EDHs) are responsible for the periplasmic oxidation of a broad variety of volatile organic compounds (VOCs). Depending on the availability of rare earth elements (REEs) of the lanthanide series...

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Autores principales:	Matthias Wehrmann, Charlotte Berthelot, Patrick Billard, Janosch Klebensberger
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	lanthanides LuxR-type regulator PQQ PedR2 PedS2 Pseudomonas putida Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/07907488a1de4183a81a2572b4f7aa3c
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spelling	oai:doaj.org-article:07907488a1de4183a81a2572b4f7aa3c2021-11-15T15:25:50ZThe PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT244010.1128/mSphere.00376-182379-5042https://doaj.org/article/07907488a1de4183a81a2572b4f7aa3c2018-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00376-18https://doaj.org/toc/2379-5042ABSTRACT In Pseudomonas putida KT2440, two pyrroloquinoline quinone-dependent ethanol dehydrogenases (PQQ-EDHs) are responsible for the periplasmic oxidation of a broad variety of volatile organic compounds (VOCs). Depending on the availability of rare earth elements (REEs) of the lanthanide series (Ln3+), we have recently reported that the transcription of the genes encoding the Ca2+-utilizing enzyme PedE and the Ln3+-utilizing enzyme PedH are inversely regulated. With adaptive evolution experiments, site-specific mutations, transcriptional reporter fusions, and complementation approaches, we now demonstrate that the PedS2/PedR2 (PP_2671/PP_2672) two-component system (TCS) plays a central role in the observed REE-mediated switch of PQQ-EDHs in P. putida. We provide evidence that in the absence of lanthanum (La3+), the sensor histidine kinase PedS2 phosphorylates its cognate LuxR-type response regulator PedR2, which in turn not only activates pedE gene transcription but is also involved in repression of pedH. Our data further suggest that the presence of La3+ lowers kinase activity of PedS2, either by the direct binding of the metal ions to the periplasmic region of PedS2 or by an uncharacterized indirect interaction, leading to reduced levels of phosphorylated PedR2. Consequently, the decreasing pedE expression and concomitant alleviation of pedH repression causes—in conjunction with the transcriptional activation of the pedH gene by a yet unknown regulatory module—the Ln3+-dependent transition from PedE- to PedH-catalyzed oxidation of alcoholic VOCs. IMPORTANCE The function of lanthanides for methanotrophic and methylotrophic bacteria is gaining increasing attention, while knowledge about the role of rare earth elements (REEs) in nonmethylotrophic bacteria is still limited. The present study investigates the recently described differential expression of the two PQQ-EDHs of P. putida in response to lanthanides. We demonstrate that a specific TCS is crucial for their inverse regulation and provide evidence for a dual regulatory function of the LuxR-type response regulator involved. Thus, our study represents the first detailed characterization of the molecular mechanism underlying the REE switch of PQQ-EDHs in a nonmethylotrophic bacterium and stimulates subsequent investigations for the identification of additional genes or phenotypic traits that might be coregulated during REE-dependent niche adaptation.Matthias WehrmannCharlotte BerthelotPatrick BillardJanosch KlebensbergerAmerican Society for MicrobiologyarticlelanthanidesLuxR-type regulatorPQQPedR2PedS2Pseudomonas putidaMicrobiologyQR1-502ENmSphere, Vol 3, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	lanthanides LuxR-type regulator PQQ PedR2 PedS2 Pseudomonas putida Microbiology QR1-502
spellingShingle	lanthanides LuxR-type regulator PQQ PedR2 PedS2 Pseudomonas putida Microbiology QR1-502 Matthias Wehrmann Charlotte Berthelot Patrick Billard Janosch Klebensberger The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
description	ABSTRACT In Pseudomonas putida KT2440, two pyrroloquinoline quinone-dependent ethanol dehydrogenases (PQQ-EDHs) are responsible for the periplasmic oxidation of a broad variety of volatile organic compounds (VOCs). Depending on the availability of rare earth elements (REEs) of the lanthanide series (Ln3+), we have recently reported that the transcription of the genes encoding the Ca2+-utilizing enzyme PedE and the Ln3+-utilizing enzyme PedH are inversely regulated. With adaptive evolution experiments, site-specific mutations, transcriptional reporter fusions, and complementation approaches, we now demonstrate that the PedS2/PedR2 (PP_2671/PP_2672) two-component system (TCS) plays a central role in the observed REE-mediated switch of PQQ-EDHs in P. putida. We provide evidence that in the absence of lanthanum (La3+), the sensor histidine kinase PedS2 phosphorylates its cognate LuxR-type response regulator PedR2, which in turn not only activates pedE gene transcription but is also involved in repression of pedH. Our data further suggest that the presence of La3+ lowers kinase activity of PedS2, either by the direct binding of the metal ions to the periplasmic region of PedS2 or by an uncharacterized indirect interaction, leading to reduced levels of phosphorylated PedR2. Consequently, the decreasing pedE expression and concomitant alleviation of pedH repression causes—in conjunction with the transcriptional activation of the pedH gene by a yet unknown regulatory module—the Ln3+-dependent transition from PedE- to PedH-catalyzed oxidation of alcoholic VOCs. IMPORTANCE The function of lanthanides for methanotrophic and methylotrophic bacteria is gaining increasing attention, while knowledge about the role of rare earth elements (REEs) in nonmethylotrophic bacteria is still limited. The present study investigates the recently described differential expression of the two PQQ-EDHs of P. putida in response to lanthanides. We demonstrate that a specific TCS is crucial for their inverse regulation and provide evidence for a dual regulatory function of the LuxR-type response regulator involved. Thus, our study represents the first detailed characterization of the molecular mechanism underlying the REE switch of PQQ-EDHs in a nonmethylotrophic bacterium and stimulates subsequent investigations for the identification of additional genes or phenotypic traits that might be coregulated during REE-dependent niche adaptation.
format	article
author	Matthias Wehrmann Charlotte Berthelot Patrick Billard Janosch Klebensberger
author_facet	Matthias Wehrmann Charlotte Berthelot Patrick Billard Janosch Klebensberger
author_sort	Matthias Wehrmann
title	The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_short	The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_full	The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_fullStr	The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_full_unstemmed	The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_sort	peds2/pedr2 two-component system is crucial for the rare earth element switch in <named-content content-type="genus-species">pseudomonas putida</named-content> kt2440
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/07907488a1de4183a81a2572b4f7aa3c
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The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440

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