Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics

Autores
Shimizu, Takayuki; Ida, Tomoaki; Antelo, Giuliano Tomás; Ihara, Yuta; Fakhoury, Joseph N; Masuda, Shinji; Giedroc, David P; Akaike, Takaaki; Capdevila, Daiana Andrea; Masuda, Tatsuru
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Sulfide plays essential roles in controlling various physiological activities in almost all organisms. Although recent evidence has demonstrated that sulfide is endogenously generated and metabolized into polysulfides inside the cells, the relationship between polysulfides metabolism and polysulfides-sensing mechanisms is not well understood. To better define this interplay between polysulfide metabolism and polysulfide sensing in cells, we investigated the role of polysulfide-metabolizing enzymes such as SQR (sulfide:quinone reductase) on the temporal dynamics of cellular polysulfides speciation and on the transcriptional regulation by the persulfide-responsive transcription factor SqrR in Rhodobacter capsulatus. We show that disruption of the sqr gene resulted in the loss of SqrR repression by exogenous sulfide at longer culture times, which impacts the speciation of intracellular polysulfides of Δsqr vs. wild-type strains. Both the attenuated response of SqrR and the change in polysulfide dynamics of the Δsqr strain is fully reversed by the addition to cells of cystine-derived polysulfides, but not by glutathione disulfide (GSSG)-derived polysulfides. Furthermore, cysteine persulfide (CysSSH) yields a higher rate of oxidation of SqrR relative to glutathione persulfide (GSSH), which leads to DNA dissociation in vitro. The oxidation of SqrR was confirmed by a mass spectrometry-based kinetic profiling strategy that showed distinct polysulfide-crosslinked products obtained with CysSSH vs. GSSH. Taken together, these results establish a novel association between the metabolism of polysulfides and the mechanisms for polysulfide sensing inside the cells.
Fil: Shimizu, Takayuki. University of Tokyo; Japón
Fil: Ida, Tomoaki. Tohoku University; Japón
Fil: Antelo, Giuliano Tomás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Indiana University; Estados Unidos
Fil: Ihara, Yuta. Tokyo Institute Of Technology; Japón
Fil: Fakhoury, Joseph N. Indiana University; Estados Unidos
Fil: Masuda, Shinji. Tokyo Institute Of Technology; Japón
Fil: Giedroc, David P. Indiana University; Estados Unidos
Fil: Akaike, Takaaki. Tohoku University; Japón
Fil: Capdevila, Daiana Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Indiana University; Estados Unidos
Fil: Masuda, Tatsuru. University of Tokyo; Japón
Materia
POLYSULFIDE
SULFUR
METABOLISM
SIGNAL
TRANSDUCTION
PROTEOBACTERIA
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/229514
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/229514
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamicsShimizu, TakayukiIda, TomoakiAntelo, Giuliano TomásIhara, YutaFakhoury, Joseph NMasuda, ShinjiGiedroc, David PAkaike, TakaakiCapdevila, Daiana AndreaMasuda, TatsuruPOLYSULFIDESULFURMETABOLISMSIGNALTRANSDUCTIONPROTEOBACTERIAhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Sulfide plays essential roles in controlling various physiological activities in almost all organisms. Although recent evidence has demonstrated that sulfide is endogenously generated and metabolized into polysulfides inside the cells, the relationship between polysulfides metabolism and polysulfides-sensing mechanisms is not well understood. To better define this interplay between polysulfide metabolism and polysulfide sensing in cells, we investigated the role of polysulfide-metabolizing enzymes such as SQR (sulfide:quinone reductase) on the temporal dynamics of cellular polysulfides speciation and on the transcriptional regulation by the persulfide-responsive transcription factor SqrR in Rhodobacter capsulatus. We show that disruption of the sqr gene resulted in the loss of SqrR repression by exogenous sulfide at longer culture times, which impacts the speciation of intracellular polysulfides of Δsqr vs. wild-type strains. Both the attenuated response of SqrR and the change in polysulfide dynamics of the Δsqr strain is fully reversed by the addition to cells of cystine-derived polysulfides, but not by glutathione disulfide (GSSG)-derived polysulfides. Furthermore, cysteine persulfide (CysSSH) yields a higher rate of oxidation of SqrR relative to glutathione persulfide (GSSH), which leads to DNA dissociation in vitro. The oxidation of SqrR was confirmed by a mass spectrometry-based kinetic profiling strategy that showed distinct polysulfide-crosslinked products obtained with CysSSH vs. GSSH. Taken together, these results establish a novel association between the metabolism of polysulfides and the mechanisms for polysulfide sensing inside the cells.Fil: Shimizu, Takayuki. University of Tokyo; JapónFil: Ida, Tomoaki. Tohoku University; JapónFil: Antelo, Giuliano Tomás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Indiana University; Estados UnidosFil: Ihara, Yuta. Tokyo Institute Of Technology; JapónFil: Fakhoury, Joseph N. Indiana University; Estados UnidosFil: Masuda, Shinji. Tokyo Institute Of Technology; JapónFil: Giedroc, David P. Indiana University; Estados UnidosFil: Akaike, Takaaki. Tohoku University; JapónFil: Capdevila, Daiana Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Indiana University; Estados UnidosFil: Masuda, Tatsuru. University of Tokyo; JapónNational Academy of Sciences2023-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/229514Shimizu, Takayuki; Ida, Tomoaki; Antelo, Giuliano Tomás; Ihara, Yuta; Fakhoury, Joseph N; et al.; Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics; National Academy of Sciences; PNAS Nexus; 2; 3; 2-2023; 1-272752-6542CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/pnasnexus/advance-article/doi/10.1093/pnasnexus/pgad048/7034213info:eu-repo/semantics/altIdentifier/doi/10.1093/pnasnexus/pgad048info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:20:19Zoai:ri.conicet.gov.ar:11336/229514instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-22 11:20:20.17CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
title Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
spellingShingle Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
Shimizu, Takayuki
POLYSULFIDE
SULFUR
METABOLISM
SIGNAL
TRANSDUCTION
PROTEOBACTERIA
title_short Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
title_full Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
title_fullStr Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
title_full_unstemmed Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
title_sort Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics
dc.creator.none.fl_str_mv Shimizu, Takayuki
Ida, Tomoaki
Antelo, Giuliano Tomás
Ihara, Yuta
Fakhoury, Joseph N
Masuda, Shinji
Giedroc, David P
Akaike, Takaaki
Capdevila, Daiana Andrea
Masuda, Tatsuru
author Shimizu, Takayuki
author_facet Shimizu, Takayuki
Ida, Tomoaki
Antelo, Giuliano Tomás
Ihara, Yuta
Fakhoury, Joseph N
Masuda, Shinji
Giedroc, David P
Akaike, Takaaki
Capdevila, Daiana Andrea
Masuda, Tatsuru
author_role author
author2 Ida, Tomoaki
Antelo, Giuliano Tomás
Ihara, Yuta
Fakhoury, Joseph N
Masuda, Shinji
Giedroc, David P
Akaike, Takaaki
Capdevila, Daiana Andrea
Masuda, Tatsuru
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv POLYSULFIDE
SULFUR
METABOLISM
SIGNAL
TRANSDUCTION
PROTEOBACTERIA
topic POLYSULFIDE
SULFUR
METABOLISM
SIGNAL
TRANSDUCTION
PROTEOBACTERIA
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Sulfide plays essential roles in controlling various physiological activities in almost all organisms. Although recent evidence has demonstrated that sulfide is endogenously generated and metabolized into polysulfides inside the cells, the relationship between polysulfides metabolism and polysulfides-sensing mechanisms is not well understood. To better define this interplay between polysulfide metabolism and polysulfide sensing in cells, we investigated the role of polysulfide-metabolizing enzymes such as SQR (sulfide:quinone reductase) on the temporal dynamics of cellular polysulfides speciation and on the transcriptional regulation by the persulfide-responsive transcription factor SqrR in Rhodobacter capsulatus. We show that disruption of the sqr gene resulted in the loss of SqrR repression by exogenous sulfide at longer culture times, which impacts the speciation of intracellular polysulfides of Δsqr vs. wild-type strains. Both the attenuated response of SqrR and the change in polysulfide dynamics of the Δsqr strain is fully reversed by the addition to cells of cystine-derived polysulfides, but not by glutathione disulfide (GSSG)-derived polysulfides. Furthermore, cysteine persulfide (CysSSH) yields a higher rate of oxidation of SqrR relative to glutathione persulfide (GSSH), which leads to DNA dissociation in vitro. The oxidation of SqrR was confirmed by a mass spectrometry-based kinetic profiling strategy that showed distinct polysulfide-crosslinked products obtained with CysSSH vs. GSSH. Taken together, these results establish a novel association between the metabolism of polysulfides and the mechanisms for polysulfide sensing inside the cells.
Fil: Shimizu, Takayuki. University of Tokyo; Japón
Fil: Ida, Tomoaki. Tohoku University; Japón
Fil: Antelo, Giuliano Tomás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Indiana University; Estados Unidos
Fil: Ihara, Yuta. Tokyo Institute Of Technology; Japón
Fil: Fakhoury, Joseph N. Indiana University; Estados Unidos
Fil: Masuda, Shinji. Tokyo Institute Of Technology; Japón
Fil: Giedroc, David P. Indiana University; Estados Unidos
Fil: Akaike, Takaaki. Tohoku University; Japón
Fil: Capdevila, Daiana Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Indiana University; Estados Unidos
Fil: Masuda, Tatsuru. University of Tokyo; Japón
description Sulfide plays essential roles in controlling various physiological activities in almost all organisms. Although recent evidence has demonstrated that sulfide is endogenously generated and metabolized into polysulfides inside the cells, the relationship between polysulfides metabolism and polysulfides-sensing mechanisms is not well understood. To better define this interplay between polysulfide metabolism and polysulfide sensing in cells, we investigated the role of polysulfide-metabolizing enzymes such as SQR (sulfide:quinone reductase) on the temporal dynamics of cellular polysulfides speciation and on the transcriptional regulation by the persulfide-responsive transcription factor SqrR in Rhodobacter capsulatus. We show that disruption of the sqr gene resulted in the loss of SqrR repression by exogenous sulfide at longer culture times, which impacts the speciation of intracellular polysulfides of Δsqr vs. wild-type strains. Both the attenuated response of SqrR and the change in polysulfide dynamics of the Δsqr strain is fully reversed by the addition to cells of cystine-derived polysulfides, but not by glutathione disulfide (GSSG)-derived polysulfides. Furthermore, cysteine persulfide (CysSSH) yields a higher rate of oxidation of SqrR relative to glutathione persulfide (GSSH), which leads to DNA dissociation in vitro. The oxidation of SqrR was confirmed by a mass spectrometry-based kinetic profiling strategy that showed distinct polysulfide-crosslinked products obtained with CysSSH vs. GSSH. Taken together, these results establish a novel association between the metabolism of polysulfides and the mechanisms for polysulfide sensing inside the cells.
publishDate 2023
dc.date.none.fl_str_mv 2023-02
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/229514
Shimizu, Takayuki; Ida, Tomoaki; Antelo, Giuliano Tomás; Ihara, Yuta; Fakhoury, Joseph N; et al.; Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics; National Academy of Sciences; PNAS Nexus; 2; 3; 2-2023; 1-27
2752-6542
CONICET Digital
CONICET
url http://hdl.handle.net/11336/229514
identifier_str_mv Shimizu, Takayuki; Ida, Tomoaki; Antelo, Giuliano Tomás; Ihara, Yuta; Fakhoury, Joseph N; et al.; Polysulfide metabolizing enzymes influence SqrR-mediated sulfide-induced transcription by impacting intracellular polysulfide dynamics; National Academy of Sciences; PNAS Nexus; 2; 3; 2-2023; 1-27
2752-6542
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/pnasnexus/advance-article/doi/10.1093/pnasnexus/pgad048/7034213
info:eu-repo/semantics/altIdentifier/doi/10.1093/pnasnexus/pgad048
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.229304

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