Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803

ABSTRACT Methylglyoxal (MG) is a detrimental metabolic by-product that threatens most organisms (in humans MG causes diabetes). MG is predominantly detoxified by the glyoxalase pathway. This process begins with the conjugation of MG with glutathione (GSH), yielding a hemithioacetal product that is s...

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Autores principales:	Xavier Kammerscheit, Arnaud Hecker, Nicolas Rouhier, Franck Chauvat, Corinne Cassier-Chauvat
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	cyanobacteria detoxification enzyme assay glutathione transferase glyoxalase pathway in vivo analysis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/af4ab9315a4c408d9b869f032814fa79
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spelling	oai:doaj.org-article:af4ab9315a4c408d9b869f032814fa792021-11-15T15:56:43ZMethylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 680310.1128/mBio.00882-202150-7511https://doaj.org/article/af4ab9315a4c408d9b869f032814fa792020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00882-20https://doaj.org/toc/2150-7511ABSTRACT Methylglyoxal (MG) is a detrimental metabolic by-product that threatens most organisms (in humans MG causes diabetes). MG is predominantly detoxified by the glyoxalase pathway. This process begins with the conjugation of MG with glutathione (GSH), yielding a hemithioacetal product that is subsequently transformed by the glyoxalase enzymes into d-lactate and GSH. MG has been overlooked in photosynthetic organisms, although they inevitably produce it not only by the catabolism of sugars, lipids, and amino acids, as do heterotrophic organisms, but also by their active photoautotrophic metabolism. This is especially true for cyanobacteria that are regarded as having developed photosynthesis and GSH-dependent enzymes to detoxify the reactive oxygen species produced by their photosynthesis (CO2 assimilation) and respiration (glucose catabolism), which they perform in the same cell compartment. In this study, we used a combination of in vivo and in vitro approaches to characterize a logical, but as yet never described, link between MG detoxification and a (prokaryotic) representative of the evolutionarily conserved glutathione transferase (GST) detoxification enzymes. We show that the Sll0067 GST of the model cyanobacterium Synechocystis sp. strain PCC 6803 plays a prominent role in MG tolerance and detoxification, unlike the other five GSTs of this organism. Sll0067 catalyzes the conjugation of MG with GSH to initiate its elimination driven by glyoxalases. These results are novel because the conjugation of MG with GSH is always described as nonenzymatic. They will certainly stimulate the analysis of Sll0067 orthologs from other organisms with possible impacts on human health (development of biomarkers or drugs) and/or agriculture. IMPORTANCE In most organisms, methylglyoxal (MG), a toxic metabolite by-product that causes diabetes in humans, is predominantly detoxified by the glyoxalase enzymes. This process begins with the so-called “spontaneous” conjugation of MG with the cytoprotectant metabolite glutathione (GSH). In this study, we unravel a logical, but as yet unsuspected, link between MG detoxification and a (prokaryotic) representative of the ubiquitous glutathione transferase (GST) enzymes. We show that a GST of a model cyanobacterium plays a prominent role in the detoxification of MG in catalyzing its conjugation with GSH. This finding is important because this reaction, always regarded as nonenzymatic, could exist in plants and/or human and thus have an impact on agriculture and/or human health.Xavier KammerscheitArnaud HeckerNicolas RouhierFranck ChauvatCorinne Cassier-ChauvatAmerican Society for Microbiologyarticlecyanobacteriadetoxificationenzyme assayglutathione transferaseglyoxalase pathwayin vivo analysisMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	cyanobacteria detoxification enzyme assay glutathione transferase glyoxalase pathway in vivo analysis Microbiology QR1-502
spellingShingle	cyanobacteria detoxification enzyme assay glutathione transferase glyoxalase pathway in vivo analysis Microbiology QR1-502 Xavier Kammerscheit Arnaud Hecker Nicolas Rouhier Franck Chauvat Corinne Cassier-Chauvat Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803
description	ABSTRACT Methylglyoxal (MG) is a detrimental metabolic by-product that threatens most organisms (in humans MG causes diabetes). MG is predominantly detoxified by the glyoxalase pathway. This process begins with the conjugation of MG with glutathione (GSH), yielding a hemithioacetal product that is subsequently transformed by the glyoxalase enzymes into d-lactate and GSH. MG has been overlooked in photosynthetic organisms, although they inevitably produce it not only by the catabolism of sugars, lipids, and amino acids, as do heterotrophic organisms, but also by their active photoautotrophic metabolism. This is especially true for cyanobacteria that are regarded as having developed photosynthesis and GSH-dependent enzymes to detoxify the reactive oxygen species produced by their photosynthesis (CO2 assimilation) and respiration (glucose catabolism), which they perform in the same cell compartment. In this study, we used a combination of in vivo and in vitro approaches to characterize a logical, but as yet never described, link between MG detoxification and a (prokaryotic) representative of the evolutionarily conserved glutathione transferase (GST) detoxification enzymes. We show that the Sll0067 GST of the model cyanobacterium Synechocystis sp. strain PCC 6803 plays a prominent role in MG tolerance and detoxification, unlike the other five GSTs of this organism. Sll0067 catalyzes the conjugation of MG with GSH to initiate its elimination driven by glyoxalases. These results are novel because the conjugation of MG with GSH is always described as nonenzymatic. They will certainly stimulate the analysis of Sll0067 orthologs from other organisms with possible impacts on human health (development of biomarkers or drugs) and/or agriculture. IMPORTANCE In most organisms, methylglyoxal (MG), a toxic metabolite by-product that causes diabetes in humans, is predominantly detoxified by the glyoxalase enzymes. This process begins with the so-called “spontaneous” conjugation of MG with the cytoprotectant metabolite glutathione (GSH). In this study, we unravel a logical, but as yet unsuspected, link between MG detoxification and a (prokaryotic) representative of the ubiquitous glutathione transferase (GST) enzymes. We show that a GST of a model cyanobacterium plays a prominent role in the detoxification of MG in catalyzing its conjugation with GSH. This finding is important because this reaction, always regarded as nonenzymatic, could exist in plants and/or human and thus have an impact on agriculture and/or human health.
format	article
author	Xavier Kammerscheit Arnaud Hecker Nicolas Rouhier Franck Chauvat Corinne Cassier-Chauvat
author_facet	Xavier Kammerscheit Arnaud Hecker Nicolas Rouhier Franck Chauvat Corinne Cassier-Chauvat
author_sort	Xavier Kammerscheit
title	Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803
title_short	Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803
title_full	Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803
title_fullStr	Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803
title_full_unstemmed	Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803
title_sort	methylglyoxal detoxification revisited: role of glutathione transferase in model cyanobacterium <italic toggle="yes">synechocystis</italic> sp. strain pcc 6803
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/af4ab9315a4c408d9b869f032814fa79
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Methylglyoxal Detoxification Revisited: Role of Glutathione Transferase in Model Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803

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