BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress

Abstract To cope with toxic levels of H2S, the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens employ the bigR operon to oxidize H2S into sulfite. The bigR operon is regulated by the transcriptional repressor BigR and it encodes a bifunctional sulfur transferase (ST) and sulfur diox...

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Main Authors: Nayara Patricia Vieira de Lira, Bianca Alves Pauletti, Ana Carolina Marques, Carlos Alberto Perez, Raquel Caserta, Alessandra Alves de Souza, Aníbal Eugênio Vercesi, Adriana Franco Paes Leme, Celso Eduardo Benedetti
Format: Article
Language:English
Published: Nature Publishing Group 2018-02-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-018-21974-x
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spelling doaj-b0a56edd1d12406d99e801a4e37069422020-12-08T06:07:37ZengNature Publishing GroupScientific Reports2045-23222018-02-018111310.1038/s41598-018-21974-xBigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stressNayara Patricia Vieira de Lira0Bianca Alves Pauletti1Ana Carolina Marques2Carlos Alberto Perez3Raquel Caserta4Alessandra Alves de Souza5Aníbal Eugênio Vercesi6Adriana Franco Paes Leme7Celso Eduardo Benedetti8Brazilian Biosciences National Laboratory (LNBio), Brazilian Center for Research in Energy and Materials (CNPEM)Brazilian Biosciences National Laboratory (LNBio), Brazilian Center for Research in Energy and Materials (CNPEM)Department of Clinical Pathology, Faculty of Medical Sciences, State University of CampinasBrazilian Synchrotron Light Laboratory (LNLS), Brazilian Center for Research in Energy and Materials (CNPEM)Agronomic Institute of Campinas, Citriculture Research Center ‘Sylvio Moreira’Agronomic Institute of Campinas, Citriculture Research Center ‘Sylvio Moreira’Department of Clinical Pathology, Faculty of Medical Sciences, State University of CampinasBrazilian Biosciences National Laboratory (LNBio), Brazilian Center for Research in Energy and Materials (CNPEM)Brazilian Biosciences National Laboratory (LNBio), Brazilian Center for Research in Energy and Materials (CNPEM)Abstract To cope with toxic levels of H2S, the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens employ the bigR operon to oxidize H2S into sulfite. The bigR operon is regulated by the transcriptional repressor BigR and it encodes a bifunctional sulfur transferase (ST) and sulfur dioxygenase (SDO) enzyme, Blh, required for H2S oxidation and bacterial growth under hypoxia. However, how Blh operates to enhance bacterial survival under hypoxia and how BigR is deactivated to derepress operon transcription is unknown. Here, we show that the ST and SDO activities of Blh are in vitro coupled and necessary to oxidize sulfide into sulfite, and that Blh is critical to maintain the oxygen flux during A. tumefaciens respiration when oxygen becomes limited to cells. We also show that H2S and polysulfides inactivate BigR leading to operon transcription. Moreover, we show that sulfite, which is produced by Blh in the ST and SDO reactions, is toxic to Citrus sinensis and that X. fastidiosa-infected plants accumulate sulfite and higher transcript levels of sulfite detoxification enzymes, suggesting that they are under sulfite stress. These results indicate that BigR acts as a sulfide sensor in the H2S oxidation mechanism that allows pathogens to colonize plant tissues where oxygen is a limiting factor.https://doi.org/10.1038/s41598-018-21974-x
collection DOAJ
language English
format Article
sources DOAJ
author Nayara Patricia Vieira de Lira
Bianca Alves Pauletti
Ana Carolina Marques
Carlos Alberto Perez
Raquel Caserta
Alessandra Alves de Souza
Aníbal Eugênio Vercesi
Adriana Franco Paes Leme
Celso Eduardo Benedetti
spellingShingle Nayara Patricia Vieira de Lira
Bianca Alves Pauletti
Ana Carolina Marques
Carlos Alberto Perez
Raquel Caserta
Alessandra Alves de Souza
Aníbal Eugênio Vercesi
Adriana Franco Paes Leme
Celso Eduardo Benedetti
BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
Scientific Reports
author_facet Nayara Patricia Vieira de Lira
Bianca Alves Pauletti
Ana Carolina Marques
Carlos Alberto Perez
Raquel Caserta
Alessandra Alves de Souza
Aníbal Eugênio Vercesi
Adriana Franco Paes Leme
Celso Eduardo Benedetti
author_sort Nayara Patricia Vieira de Lira
title BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
title_short BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
title_full BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
title_fullStr BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
title_full_unstemmed BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
title_sort bigr is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2018-02-01
description Abstract To cope with toxic levels of H2S, the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens employ the bigR operon to oxidize H2S into sulfite. The bigR operon is regulated by the transcriptional repressor BigR and it encodes a bifunctional sulfur transferase (ST) and sulfur dioxygenase (SDO) enzyme, Blh, required for H2S oxidation and bacterial growth under hypoxia. However, how Blh operates to enhance bacterial survival under hypoxia and how BigR is deactivated to derepress operon transcription is unknown. Here, we show that the ST and SDO activities of Blh are in vitro coupled and necessary to oxidize sulfide into sulfite, and that Blh is critical to maintain the oxygen flux during A. tumefaciens respiration when oxygen becomes limited to cells. We also show that H2S and polysulfides inactivate BigR leading to operon transcription. Moreover, we show that sulfite, which is produced by Blh in the ST and SDO reactions, is toxic to Citrus sinensis and that X. fastidiosa-infected plants accumulate sulfite and higher transcript levels of sulfite detoxification enzymes, suggesting that they are under sulfite stress. These results indicate that BigR acts as a sulfide sensor in the H2S oxidation mechanism that allows pathogens to colonize plant tissues where oxygen is a limiting factor.
url https://doi.org/10.1038/s41598-018-21974-x
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