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Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid

Nitropropionic acid (NPA) is a widely distributed naturally occurring nitroaliphatic toxin produced by leguminous plants and fungi. The Southern green shield bug feeds on leguminous plants and shows no symptoms of intoxication. Likewise, its gut-associated microorganisms are subjected to high levels...

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Autores principales: Rogowska-van der Molen, Magda A., Nagornîi, Dmitrii, Coolen, Silvia, de Graaf, Rob M., Berben, Tom, van Alen, Theo, Janssen, Mathilde A. C. H., Rutjes, Floris P. J. T., Jansen, Robert S., Welte, Cornelia U.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9552603/
https://www.ncbi.nlm.nih.gov/pubmed/36154165
http://dx.doi.org/10.1128/aem.00719-22
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author Rogowska-van der Molen, Magda A.
Nagornîi, Dmitrii
Coolen, Silvia
de Graaf, Rob M.
Berben, Tom
van Alen, Theo
Janssen, Mathilde A. C. H.
Rutjes, Floris P. J. T.
Jansen, Robert S.
Welte, Cornelia U.
author_facet Rogowska-van der Molen, Magda A.
Nagornîi, Dmitrii
Coolen, Silvia
de Graaf, Rob M.
Berben, Tom
van Alen, Theo
Janssen, Mathilde A. C. H.
Rutjes, Floris P. J. T.
Jansen, Robert S.
Welte, Cornelia U.
author_sort Rogowska-van der Molen, Magda A.
collection PubMed
description Nitropropionic acid (NPA) is a widely distributed naturally occurring nitroaliphatic toxin produced by leguminous plants and fungi. The Southern green shield bug feeds on leguminous plants and shows no symptoms of intoxication. Likewise, its gut-associated microorganisms are subjected to high levels of this toxic compound. In this study, we isolated a bacterium from this insect's gut system, classified as Pseudomonas sp. strain Nvir, that was highly resistant to NPA and was fully degrading it to inorganic nitrogen compounds and carbon dioxide. In order to understand the metabolic fate of NPA, we traced the fate of all atoms of the NPA molecule using isotope tracing experiments with [(15)N]NPA and [1-(13)C]NPA, in addition to experiments with uniformly (13)C-labeled biomass that was used to follow the incorporation of (12)C atoms from [U-(12)C]NPA into tricarboxylic acid cycle intermediates. With the help of genomics and transcriptomics, we uncovered the isolate’s NPA degradation pathway, which involves a putative propionate-3-nitronate monooxygenase responsible for the first step of NPA degradation. The discovered protein shares only 32% sequence identity with previously described propionate-3-nitronate monooxygenases. Finally, we advocate that NPA-degrading bacteria might find application in biotechnology, and their unique enzymes might be used in biosynthesis, bioremediation, and in dealing with postharvest NPA contamination in economically important products. IMPORTANCE Plants have evolved sophisticated chemical defense mechanisms, such as the production of plant toxins in order to deter herbivores. One example of such a plant toxin is nitropropionic acid (NPA), which is produced by leguminous plants and also by certain fungi. In this project, we have isolated a bacterium from the intestinal tract of a pest insect, the Southern green shield bug, that is able to degrade NPA. Through a multiomics approach, we identified the respective metabolic pathway and determined the metabolic fate of all atoms of the NPA molecule. In addition, we provide a new genetic marker that can be used for genome mining toward NPA degradation. The discovery of degradation pathways of plant toxins by environmental bacteria opens new possibilities for pretreatment of contaminated food and feed sources and characterization of understudied enzymes allows their broad application in biotechnology.
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spelling pubmed-95526032022-10-12 Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid Rogowska-van der Molen, Magda A. Nagornîi, Dmitrii Coolen, Silvia de Graaf, Rob M. Berben, Tom van Alen, Theo Janssen, Mathilde A. C. H. Rutjes, Floris P. J. T. Jansen, Robert S. Welte, Cornelia U. Appl Environ Microbiol Environmental Microbiology Nitropropionic acid (NPA) is a widely distributed naturally occurring nitroaliphatic toxin produced by leguminous plants and fungi. The Southern green shield bug feeds on leguminous plants and shows no symptoms of intoxication. Likewise, its gut-associated microorganisms are subjected to high levels of this toxic compound. In this study, we isolated a bacterium from this insect's gut system, classified as Pseudomonas sp. strain Nvir, that was highly resistant to NPA and was fully degrading it to inorganic nitrogen compounds and carbon dioxide. In order to understand the metabolic fate of NPA, we traced the fate of all atoms of the NPA molecule using isotope tracing experiments with [(15)N]NPA and [1-(13)C]NPA, in addition to experiments with uniformly (13)C-labeled biomass that was used to follow the incorporation of (12)C atoms from [U-(12)C]NPA into tricarboxylic acid cycle intermediates. With the help of genomics and transcriptomics, we uncovered the isolate’s NPA degradation pathway, which involves a putative propionate-3-nitronate monooxygenase responsible for the first step of NPA degradation. The discovered protein shares only 32% sequence identity with previously described propionate-3-nitronate monooxygenases. Finally, we advocate that NPA-degrading bacteria might find application in biotechnology, and their unique enzymes might be used in biosynthesis, bioremediation, and in dealing with postharvest NPA contamination in economically important products. IMPORTANCE Plants have evolved sophisticated chemical defense mechanisms, such as the production of plant toxins in order to deter herbivores. One example of such a plant toxin is nitropropionic acid (NPA), which is produced by leguminous plants and also by certain fungi. In this project, we have isolated a bacterium from the intestinal tract of a pest insect, the Southern green shield bug, that is able to degrade NPA. Through a multiomics approach, we identified the respective metabolic pathway and determined the metabolic fate of all atoms of the NPA molecule. In addition, we provide a new genetic marker that can be used for genome mining toward NPA degradation. The discovery of degradation pathways of plant toxins by environmental bacteria opens new possibilities for pretreatment of contaminated food and feed sources and characterization of understudied enzymes allows their broad application in biotechnology. American Society for Microbiology 2022-09-26 /pmc/articles/PMC9552603/ /pubmed/36154165 http://dx.doi.org/10.1128/aem.00719-22 Text en Copyright © 2022 Rogowska-van der Molen et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Environmental Microbiology
Rogowska-van der Molen, Magda A.
Nagornîi, Dmitrii
Coolen, Silvia
de Graaf, Rob M.
Berben, Tom
van Alen, Theo
Janssen, Mathilde A. C. H.
Rutjes, Floris P. J. T.
Jansen, Robert S.
Welte, Cornelia U.
Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid
title Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid
title_full Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid
title_fullStr Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid
title_full_unstemmed Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid
title_short Insect Gut Isolate Pseudomonas sp. Strain Nvir Degrades the Toxic Plant Metabolite Nitropropionic Acid
title_sort insect gut isolate pseudomonas sp. strain nvir degrades the toxic plant metabolite nitropropionic acid
topic Environmental Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9552603/
https://www.ncbi.nlm.nih.gov/pubmed/36154165
http://dx.doi.org/10.1128/aem.00719-22
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