Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440

ABSTRACT The oxidation of alcohols and aldehydes is crucial for detoxification and efficient catabolism of various volatile organic compounds (VOCs). Thus, many Gram-negative bacteria have evolved periplasmic oxidation systems based on pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-A...

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Autores principales:	Matthias Wehrmann, Patrick Billard, Audrey Martin-Meriadec, Asfaw Zegeye, Janosch Klebensberger
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	pyrroloquinoline quinone Pseudomonas putida alcohol dehydrogenase functional redundancy gene regulation lanthanides Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b52cca99fe4a442086a1eaa5b13218f5
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spelling	oai:doaj.org-article:b52cca99fe4a442086a1eaa5b13218f52021-11-15T15:51:30ZFunctional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT244010.1128/mBio.00570-172150-7511https://doaj.org/article/b52cca99fe4a442086a1eaa5b13218f52017-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00570-17https://doaj.org/toc/2150-7511ABSTRACT The oxidation of alcohols and aldehydes is crucial for detoxification and efficient catabolism of various volatile organic compounds (VOCs). Thus, many Gram-negative bacteria have evolved periplasmic oxidation systems based on pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-ADHs) that are often functionally redundant. Here we report the first description and characterization of a lanthanide-dependent PQQ-ADH (PedH) in a nonmethylotrophic bacterium based on the use of purified enzymes from the soil-dwelling model organism Pseudomonas putida KT2440. PedH (PP_2679) exhibits enzyme activity on a range of substrates similar to that of its Ca2+-dependent counterpart PedE (PP_2674), including linear and aromatic primary and secondary alcohols, as well as aldehydes, but only in the presence of lanthanide ions, including La3+, Ce3+, Pr3+, Sm3+, or Nd3+. Reporter assays revealed that PedH not only has a catalytic function but is also involved in the transcriptional regulation of pedE and pedH, most likely acting as a sensory module. Notably, the underlying regulatory network is responsive to as little as 1 to 10 nM lanthanum, a concentration assumed to be of ecological relevance. The present study further demonstrates that the PQQ-dependent oxidation system is crucial for efficient growth with a variety of volatile alcohols. From these results, we conclude that functional redundancy and inverse regulation of PedE and PedH represent an adaptive strategy of P. putida KT2440 to optimize growth with volatile alcohols in response to the availability of different lanthanides. IMPORTANCE Because of their low bioavailability, lanthanides have long been considered biologically inert. In recent years, however, the identification of lanthanides as a cofactor in methylotrophic bacteria has attracted tremendous interest among various biological fields. The present study reveals that one of the two PQQ-ADHs produced by the model organism P. putida KT2440 also utilizes lanthanides as a cofactor, thus expanding the scope of lanthanide-employing bacteria beyond the methylotrophs. Similar to the system described in methylotrophic bacteria, a complex regulatory network is involved in lanthanide-responsive switching between the two PQQ-ADHs encoded by P. putida KT2440. We further show that the functional production of at least one of the enzymes is crucial for efficient growth with several volatile alcohols. Overall, our study provides a novel understanding of the redundancy of PQQ-ADHs observed in many organisms and further highlights the importance of lanthanides for bacterial metabolism, particularly in soil environments.Matthias WehrmannPatrick BillardAudrey Martin-MeriadecAsfaw ZegeyeJanosch KlebensbergerAmerican Society for Microbiologyarticlepyrroloquinoline quinonePseudomonas putidaalcohol dehydrogenasefunctional redundancygene regulationlanthanidesMicrobiologyQR1-502ENmBio, Vol 8, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	pyrroloquinoline quinone Pseudomonas putida alcohol dehydrogenase functional redundancy gene regulation lanthanides Microbiology QR1-502
spellingShingle	pyrroloquinoline quinone Pseudomonas putida alcohol dehydrogenase functional redundancy gene regulation lanthanides Microbiology QR1-502 Matthias Wehrmann Patrick Billard Audrey Martin-Meriadec Asfaw Zegeye Janosch Klebensberger Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440
description	ABSTRACT The oxidation of alcohols and aldehydes is crucial for detoxification and efficient catabolism of various volatile organic compounds (VOCs). Thus, many Gram-negative bacteria have evolved periplasmic oxidation systems based on pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-ADHs) that are often functionally redundant. Here we report the first description and characterization of a lanthanide-dependent PQQ-ADH (PedH) in a nonmethylotrophic bacterium based on the use of purified enzymes from the soil-dwelling model organism Pseudomonas putida KT2440. PedH (PP_2679) exhibits enzyme activity on a range of substrates similar to that of its Ca2+-dependent counterpart PedE (PP_2674), including linear and aromatic primary and secondary alcohols, as well as aldehydes, but only in the presence of lanthanide ions, including La3+, Ce3+, Pr3+, Sm3+, or Nd3+. Reporter assays revealed that PedH not only has a catalytic function but is also involved in the transcriptional regulation of pedE and pedH, most likely acting as a sensory module. Notably, the underlying regulatory network is responsive to as little as 1 to 10 nM lanthanum, a concentration assumed to be of ecological relevance. The present study further demonstrates that the PQQ-dependent oxidation system is crucial for efficient growth with a variety of volatile alcohols. From these results, we conclude that functional redundancy and inverse regulation of PedE and PedH represent an adaptive strategy of P. putida KT2440 to optimize growth with volatile alcohols in response to the availability of different lanthanides. IMPORTANCE Because of their low bioavailability, lanthanides have long been considered biologically inert. In recent years, however, the identification of lanthanides as a cofactor in methylotrophic bacteria has attracted tremendous interest among various biological fields. The present study reveals that one of the two PQQ-ADHs produced by the model organism P. putida KT2440 also utilizes lanthanides as a cofactor, thus expanding the scope of lanthanide-employing bacteria beyond the methylotrophs. Similar to the system described in methylotrophic bacteria, a complex regulatory network is involved in lanthanide-responsive switching between the two PQQ-ADHs encoded by P. putida KT2440. We further show that the functional production of at least one of the enzymes is crucial for efficient growth with several volatile alcohols. Overall, our study provides a novel understanding of the redundancy of PQQ-ADHs observed in many organisms and further highlights the importance of lanthanides for bacterial metabolism, particularly in soil environments.
format	article
author	Matthias Wehrmann Patrick Billard Audrey Martin-Meriadec Asfaw Zegeye Janosch Klebensberger
author_facet	Matthias Wehrmann Patrick Billard Audrey Martin-Meriadec Asfaw Zegeye Janosch Klebensberger
author_sort	Matthias Wehrmann
title	Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440
title_short	Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440
title_full	Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440
title_fullStr	Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440
title_full_unstemmed	Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440
title_sort	functional role of lanthanides in enzymatic activity and transcriptional regulation of pyrroloquinoline quinone-dependent alcohol dehydrogenases in <italic toggle="yes">pseudomonas putida</italic> kt2440
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/b52cca99fe4a442086a1eaa5b13218f5
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Functional Role of Lanthanides in Enzymatic Activity and Transcriptional Regulation of Pyrroloquinoline Quinone-Dependent Alcohol Dehydrogenases in <italic toggle="yes">Pseudomonas putida</italic> KT2440

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