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

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 polysulfide...

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Detalles Bibliográficos
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
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:Argentina
Institución:Consejo Nacional de Investigaciones Científicas y Técnicas
Repositorio:CONICET Digital (CONICET)
Idioma:inglés
OAI Identifier:oai:ri.conicet.gov.ar:11336/229514
Acceso en línea:http://hdl.handle.net/11336/229514
Access Level:acceso abierto
Palabra clave:POLYSULFIDE
SULFUR
METABOLISM
SIGNAL
TRANSDUCTION
PROTEOBACTERIA
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
Descripción
Sumario: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.