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Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits

Although sulfite, a by-product of the degradation of many sulfur compounds, is highly reactive and can cause damage to DNA, proteins and lipids, comparatively little is known about the regulation of sulfite-oxidizing enzyme (SOEs) expression. Here we have investigated the regulation of SOE-encoding...

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Autores principales: Tan, Yi Jie Chelsea, Zhao, Chengzhi, Nasreen, Marufa, O’Rourke, Leo, Dhouib, Rabeb, Roberts, Leah, Wan, Ying, Beatson, Scott A., Kappler, Ulrike
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6527743/
https://www.ncbi.nlm.nih.gov/pubmed/31139157
http://dx.doi.org/10.3389/fmicb.2019.00960
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author Tan, Yi Jie Chelsea
Zhao, Chengzhi
Nasreen, Marufa
O’Rourke, Leo
Dhouib, Rabeb
Roberts, Leah
Wan, Ying
Beatson, Scott A.
Kappler, Ulrike
author_facet Tan, Yi Jie Chelsea
Zhao, Chengzhi
Nasreen, Marufa
O’Rourke, Leo
Dhouib, Rabeb
Roberts, Leah
Wan, Ying
Beatson, Scott A.
Kappler, Ulrike
author_sort Tan, Yi Jie Chelsea
collection PubMed
description Although sulfite, a by-product of the degradation of many sulfur compounds, is highly reactive and can cause damage to DNA, proteins and lipids, comparatively little is known about the regulation of sulfite-oxidizing enzyme (SOEs) expression. Here we have investigated the regulation of SOE-encoding genes in two species of α-Proteobacteria, Sinorhizobium meliloti and Starkeya novella, that degrade organo- and inorganic sulfur compounds, respectively, and contain unrelated types of SOEs that show different expression patterns. Our work revealed that in both cases, the molecular signal that triggers SOE gene expression is sulfite, and strong up-regulation depends on the presence of a sulfite-responsive, cognate Extracytoplasmic function (ECF) sigma factor, making sulfite oxidation a bacterial stress response. An additional RpoE1-like ECF sigma factor was also involved in the regulation, but was activated by different molecular signals, taurine (Sm) and tetrathionate (Sn), respectively, targeted different gene promoters, and also differed in the magnitude of the response generated. We therefore propose that RpoE1 is a secondary, species-specific regulator of SOE gene expression rather than a general, conserved regulatory circuit. Sulfite produced by major dissimilatory processes appeared to be the trigger for SOE gene expression in both species, as we were unable to find evidence for an increase of SOE activity in stationary growth phase. The basic regulation of bacterial sulfite oxidation by cognate ECF sigma factors is likely to be applicable to three groups of alpha and beta-Proteobacteria in which we identified similar SOE operon structures.
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spelling pubmed-65277432019-05-28 Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits Tan, Yi Jie Chelsea Zhao, Chengzhi Nasreen, Marufa O’Rourke, Leo Dhouib, Rabeb Roberts, Leah Wan, Ying Beatson, Scott A. Kappler, Ulrike Front Microbiol Microbiology Although sulfite, a by-product of the degradation of many sulfur compounds, is highly reactive and can cause damage to DNA, proteins and lipids, comparatively little is known about the regulation of sulfite-oxidizing enzyme (SOEs) expression. Here we have investigated the regulation of SOE-encoding genes in two species of α-Proteobacteria, Sinorhizobium meliloti and Starkeya novella, that degrade organo- and inorganic sulfur compounds, respectively, and contain unrelated types of SOEs that show different expression patterns. Our work revealed that in both cases, the molecular signal that triggers SOE gene expression is sulfite, and strong up-regulation depends on the presence of a sulfite-responsive, cognate Extracytoplasmic function (ECF) sigma factor, making sulfite oxidation a bacterial stress response. An additional RpoE1-like ECF sigma factor was also involved in the regulation, but was activated by different molecular signals, taurine (Sm) and tetrathionate (Sn), respectively, targeted different gene promoters, and also differed in the magnitude of the response generated. We therefore propose that RpoE1 is a secondary, species-specific regulator of SOE gene expression rather than a general, conserved regulatory circuit. Sulfite produced by major dissimilatory processes appeared to be the trigger for SOE gene expression in both species, as we were unable to find evidence for an increase of SOE activity in stationary growth phase. The basic regulation of bacterial sulfite oxidation by cognate ECF sigma factors is likely to be applicable to three groups of alpha and beta-Proteobacteria in which we identified similar SOE operon structures. Frontiers Media S.A. 2019-05-14 /pmc/articles/PMC6527743/ /pubmed/31139157 http://dx.doi.org/10.3389/fmicb.2019.00960 Text en Copyright © 2019 Tan, Zhao, Nasreen, O’Rourke, Dhouib, Roberts, Wan, Beatson and Kappler. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Tan, Yi Jie Chelsea
Zhao, Chengzhi
Nasreen, Marufa
O’Rourke, Leo
Dhouib, Rabeb
Roberts, Leah
Wan, Ying
Beatson, Scott A.
Kappler, Ulrike
Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits
title Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits
title_full Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits
title_fullStr Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits
title_full_unstemmed Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits
title_short Control of Bacterial Sulfite Detoxification by Conserved and Species-Specific Regulatory Circuits
title_sort control of bacterial sulfite detoxification by conserved and species-specific regulatory circuits
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6527743/
https://www.ncbi.nlm.nih.gov/pubmed/31139157
http://dx.doi.org/10.3389/fmicb.2019.00960
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