Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>

ABSTRACT Rhodospirillum centenum forms metabolically dormant cysts under unfavorable growth conditions such as desiccation or nutrient starvation. The development of cysts is tightly regulated and involves a cyst-repressing chemotaxis-like signal transduction pathway called the Che3 signaling cascad...

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Autores principales:	Kuang He, Vladimira Dragnea, Carl E. Bauer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/064a1d97975a466992eafc8514b276c0
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spelling	oai:doaj.org-article:064a1d97975a466992eafc8514b276c02021-11-15T15:49:02ZAdenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>10.1128/mBio.00546-152150-7511https://doaj.org/article/064a1d97975a466992eafc8514b276c02015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00546-15https://doaj.org/toc/2150-7511ABSTRACT Rhodospirillum centenum forms metabolically dormant cysts under unfavorable growth conditions such as desiccation or nutrient starvation. The development of cysts is tightly regulated and involves a cyst-repressing chemotaxis-like signal transduction pathway called the Che3 signaling cascade. The Che3 cascade is comprised of a methyl chemoreceptor (MCP3), receptor-methylating/demethylating proteins CheB3 and CheR3, two CheW3 linker proteins, a CheA3-CheY hybrid histidine kinase, and a single-domain response regulator, CheY3. In addition to Che-like components, the Che3 cascade also contains a second hybrid histidine kinase, CheS3. Recent biochemical and genetic studies show that CheA3 does not serve as a phosphor donor for CheY3; instead, CheA3 inhibits a CheS3→CheY3 two-component system by phosphorylating an inhibitory receiver domain of CheS3. In this study, we show that in addition to phosphorylation by CheA3, the phosphorylation state of CheS3 is also regulated by the cellular energy level as quantified by the molar ratio of ATP/(ATP + ADP). A 35% decrease in cellular energy is shown to occur in vivo upon a nutrient downshift that gives rise to cyst formation. When this energy decline is replicated in vitro, the phosphorylation level of CheS3 is reduced by ~75%. Finally, we also show that ADP-mediated reduction of CheS3 phosphorylation is a consequence of ADP enhancing autodephosphorylation of CheS3. IMPORTANCE Upon starvation, Rhodospirillum centenum undergoes a developmental process that forms metabolically dormant cysts, which withstand desiccation and nutritional limitation. This study explores the role of the cellular energy state as measured by the ratio of ATP to ADP as an important regulator of cyst formation in Rhodospirillum centenum. We show that R. centenum cells experience a significant reduction in ATP during cyst formation using ATP/(ATP + ADP) as a measurement. When this in vivo level of energy starvation is simulated in vitro, CheS3 phosphorylation is reduced by 75%. This profound reduction in CheS3 autophosphorylation is contrasted with a much lower 25% decrease in CheA3 phosphorylation in response to a similar downward shift in ATP/(ATP + ADP). We argue that even though adenylate energy affects all ATP-dependent enzymes to an extent, the enhanced inhibition of CheS3 activity in response to a reduction in the ATP/(ATP + ADP) ratio likely functions as an important input signal to regulate cyst development.Kuang HeVladimira DragneaCarl E. BauerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Kuang He Vladimira Dragnea Carl E. Bauer Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>
description	ABSTRACT Rhodospirillum centenum forms metabolically dormant cysts under unfavorable growth conditions such as desiccation or nutrient starvation. The development of cysts is tightly regulated and involves a cyst-repressing chemotaxis-like signal transduction pathway called the Che3 signaling cascade. The Che3 cascade is comprised of a methyl chemoreceptor (MCP3), receptor-methylating/demethylating proteins CheB3 and CheR3, two CheW3 linker proteins, a CheA3-CheY hybrid histidine kinase, and a single-domain response regulator, CheY3. In addition to Che-like components, the Che3 cascade also contains a second hybrid histidine kinase, CheS3. Recent biochemical and genetic studies show that CheA3 does not serve as a phosphor donor for CheY3; instead, CheA3 inhibits a CheS3→CheY3 two-component system by phosphorylating an inhibitory receiver domain of CheS3. In this study, we show that in addition to phosphorylation by CheA3, the phosphorylation state of CheS3 is also regulated by the cellular energy level as quantified by the molar ratio of ATP/(ATP + ADP). A 35% decrease in cellular energy is shown to occur in vivo upon a nutrient downshift that gives rise to cyst formation. When this energy decline is replicated in vitro, the phosphorylation level of CheS3 is reduced by ~75%. Finally, we also show that ADP-mediated reduction of CheS3 phosphorylation is a consequence of ADP enhancing autodephosphorylation of CheS3. IMPORTANCE Upon starvation, Rhodospirillum centenum undergoes a developmental process that forms metabolically dormant cysts, which withstand desiccation and nutritional limitation. This study explores the role of the cellular energy state as measured by the ratio of ATP to ADP as an important regulator of cyst formation in Rhodospirillum centenum. We show that R. centenum cells experience a significant reduction in ATP during cyst formation using ATP/(ATP + ADP) as a measurement. When this in vivo level of energy starvation is simulated in vitro, CheS3 phosphorylation is reduced by 75%. This profound reduction in CheS3 autophosphorylation is contrasted with a much lower 25% decrease in CheA3 phosphorylation in response to a similar downward shift in ATP/(ATP + ADP). We argue that even though adenylate energy affects all ATP-dependent enzymes to an extent, the enhanced inhibition of CheS3 activity in response to a reduction in the ATP/(ATP + ADP) ratio likely functions as an important input signal to regulate cyst development.
format	article
author	Kuang He Vladimira Dragnea Carl E. Bauer
author_facet	Kuang He Vladimira Dragnea Carl E. Bauer
author_sort	Kuang He
title	Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>
title_short	Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>
title_full	Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>
title_fullStr	Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>
title_full_unstemmed	Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>
title_sort	adenylate charge regulates sensor kinase ches<sub>3</sub> to control cyst formation in <named-content content-type="genus-species">rhodospirillum centenum</named-content>
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/064a1d97975a466992eafc8514b276c0
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Adenylate Charge Regulates Sensor Kinase CheS<sub>3</sub> To Control Cyst Formation in <named-content content-type="genus-species">Rhodospirillum centenum</named-content>

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