The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440

ABSTRACT Ever since the discovery of the first rare earth element (REE)-dependent enzyme, the physiological role of lanthanides has become an emerging field of research due to the environmental implications and biotechnological opportunities. In Pseudomonas putida KT2440, the two pyrroloquinoline qu...

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Autores principales:	Matthias Wehrmann, Maxime Toussaint, Jens Pfannstiel, Patrick Billard, Janosch Klebensberger
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	rare earth elements proteomics glycerol metabolism Pseudomonas putida PQQ PedE Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b55926830484c8b8bc0eb563d30434d
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spelling	oai:doaj.org-article:5b55926830484c8b8bc0eb563d30434d2021-11-15T15:57:03ZThe Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT244010.1128/mBio.00516-202150-7511https://doaj.org/article/5b55926830484c8b8bc0eb563d30434d2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00516-20https://doaj.org/toc/2150-7511ABSTRACT Ever since the discovery of the first rare earth element (REE)-dependent enzyme, the physiological role of lanthanides has become an emerging field of research due to the environmental implications and biotechnological opportunities. In Pseudomonas putida KT2440, the two pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-ADHs) PedE and PedH are inversely regulated in response to REE availability. This transcriptional switch is orchestrated by a complex regulatory network that includes the PedR2/PedS2 two-component system and is important for efficient growth on several alcoholic volatiles. To study whether cellular responses beyond the REE switch exist, the differential proteomic responses that occur during growth on various model carbon sources were analyzed. Apart from the Ca2+-dependent enzyme PedE, the differential abundances of most identified proteins were conditional. During growth on glycerol—and concomitant with the proteomic changes—lanthanum (La3+) availability affected different growth parameters, including the onset of logarithmic growth and final optical densities. Studies with mutant strains revealed a novel metabolic route for glycerol utilization, initiated by PedE and/or PedH activity. Upon oxidation to glycerate via glyceraldehyde, phosphorylation by the glycerate kinase GarK most likely yields glycerate-2-phosphate, which is eventually channeled into the central metabolism of the cell. This new route functions in parallel with the main degradation pathway encoded by the glpFKRD operon and provides a growth advantage to the cells by allowing an earlier onset of growth with glycerol as the sole source of carbon and energy. IMPORTANCE The biological role of REEs has long been underestimated, and research has mainly focused on methanotrophic and methylotrophic bacteria. We have recently demonstrated that P. putida, a plant growth-promoting bacterium that thrives in the rhizosphere of various food crops, possesses a REE-dependent alcohol dehydrogenase (PedH), but knowledge about REE-specific effects on physiological traits in nonmethylotrophic bacteria is still scarce. This study demonstrates that the cellular response of P. putida to lanthanum (La3+) is mostly substrate specific and that La3+ availability highly affects the growth of cells on glycerol. Further, a novel route for glycerol metabolism is identified, which is initiated by PedE and/or PedH activity and provides a growth advantage to this biotechnologically relevant organism by allowing a faster onset of growth. Overall, these findings demonstrate that lanthanides can affect physiological traits in nonmethylotrophic bacteria and might influence their competitiveness in various environmental niches.Matthias WehrmannMaxime ToussaintJens PfannstielPatrick BillardJanosch KlebensbergerAmerican Society for Microbiologyarticlerare earth elementsproteomicsglycerol metabolismPseudomonas putidaPQQPedEMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	rare earth elements proteomics glycerol metabolism Pseudomonas putida PQQ PedE Microbiology QR1-502
spellingShingle	rare earth elements proteomics glycerol metabolism Pseudomonas putida PQQ PedE Microbiology QR1-502 Matthias Wehrmann Maxime Toussaint Jens Pfannstiel Patrick Billard Janosch Klebensberger The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
description	ABSTRACT Ever since the discovery of the first rare earth element (REE)-dependent enzyme, the physiological role of lanthanides has become an emerging field of research due to the environmental implications and biotechnological opportunities. In Pseudomonas putida KT2440, the two pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-ADHs) PedE and PedH are inversely regulated in response to REE availability. This transcriptional switch is orchestrated by a complex regulatory network that includes the PedR2/PedS2 two-component system and is important for efficient growth on several alcoholic volatiles. To study whether cellular responses beyond the REE switch exist, the differential proteomic responses that occur during growth on various model carbon sources were analyzed. Apart from the Ca2+-dependent enzyme PedE, the differential abundances of most identified proteins were conditional. During growth on glycerol—and concomitant with the proteomic changes—lanthanum (La3+) availability affected different growth parameters, including the onset of logarithmic growth and final optical densities. Studies with mutant strains revealed a novel metabolic route for glycerol utilization, initiated by PedE and/or PedH activity. Upon oxidation to glycerate via glyceraldehyde, phosphorylation by the glycerate kinase GarK most likely yields glycerate-2-phosphate, which is eventually channeled into the central metabolism of the cell. This new route functions in parallel with the main degradation pathway encoded by the glpFKRD operon and provides a growth advantage to the cells by allowing an earlier onset of growth with glycerol as the sole source of carbon and energy. IMPORTANCE The biological role of REEs has long been underestimated, and research has mainly focused on methanotrophic and methylotrophic bacteria. We have recently demonstrated that P. putida, a plant growth-promoting bacterium that thrives in the rhizosphere of various food crops, possesses a REE-dependent alcohol dehydrogenase (PedH), but knowledge about REE-specific effects on physiological traits in nonmethylotrophic bacteria is still scarce. This study demonstrates that the cellular response of P. putida to lanthanum (La3+) is mostly substrate specific and that La3+ availability highly affects the growth of cells on glycerol. Further, a novel route for glycerol metabolism is identified, which is initiated by PedE and/or PedH activity and provides a growth advantage to this biotechnologically relevant organism by allowing a faster onset of growth. Overall, these findings demonstrate that lanthanides can affect physiological traits in nonmethylotrophic bacteria and might influence their competitiveness in various environmental niches.
format	article
author	Matthias Wehrmann Maxime Toussaint Jens Pfannstiel Patrick Billard Janosch Klebensberger
author_facet	Matthias Wehrmann Maxime Toussaint Jens Pfannstiel Patrick Billard Janosch Klebensberger
author_sort	Matthias Wehrmann
title	The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_short	The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_full	The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_fullStr	The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_full_unstemmed	The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440
title_sort	cellular response to lanthanum is substrate specific and reveals a novel route for glycerol metabolism in <named-content content-type="genus-species">pseudomonas putida</named-content> kt2440
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/5b55926830484c8b8bc0eb563d30434d
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The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in <named-content content-type="genus-species">Pseudomonas putida</named-content> KT2440

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