Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains

ABSTRACT Despite the myriad of different sensory domains encoded in bacterial genomes, only a few are known to control the cell cycle. Here, suppressor genetics was used to unveil the regulatory interplay between the PAS (Per-Arnt-Sim) domain protein MopJ and the uncharacterized GAF (cyclic GMP-phos...

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Autores principales:	Stefano Sanselicio, Patrick H. Viollier
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7df787c9ce1848b6ad679a40879e22b0
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spelling	oai:doaj.org-article:7df787c9ce1848b6ad679a40879e22b02021-11-15T15:41:30ZConvergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains10.1128/mBio.01415-152150-7511https://doaj.org/article/7df787c9ce1848b6ad679a40879e22b02015-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01415-15https://doaj.org/toc/2150-7511ABSTRACT Despite the myriad of different sensory domains encoded in bacterial genomes, only a few are known to control the cell cycle. Here, suppressor genetics was used to unveil the regulatory interplay between the PAS (Per-Arnt-Sim) domain protein MopJ and the uncharacterized GAF (cyclic GMP-phosphodiesterase–adenylyl cyclase–FhlA) domain protein PtsP, which resembles an alternative component of the phosphoenolpyruvate (PEP) transferase system. Both of these systems indirectly target the Caulobacter crescentus cell cycle master regulator CtrA, but in different ways. While MopJ acts on CtrA via the cell cycle kinases DivJ and DivL, which control the removal of CtrA at the G1-S transition, our data show that PtsP signals through the conserved alarmone (p)ppGpp, which prevents CtrA cycling under nutritional stress and in stationary phase. We found that PtsP interacts genetically and physically with the (p)ppGpp synthase/hydrolase SpoT and that it modulates several promoters that are directly activated by the cell cycle transcriptional regulator GcrA. Thus, parallel systems integrate nutritional and systemic signals within the cell cycle transcriptional network, converging on the essential alphaproteobacterial regulator CtrA while also affecting global cell cycle transcription in other ways. IMPORTANCE Many alphaproteobacteria divide asymmetrically, and their cell cycle progression is carefully regulated. How these bacteria control the cell cycle in response to nutrient limitation is not well understood. Here, we identify a multicomponent signaling pathway that acts on the cell cycle when nutrients become scarce in stationary phase. We show that efficient accumulation of the master cell cycle regulator CtrA in stationary-phase Caulobacter crescentus cells requires the previously identified stationary-phase/cell cycle regulator MopJ as well as the phosphoenolpyruvate protein phosphotransferase PtsP, which acts via the conserved (p)ppGpp synthase SpoT. We identify cell cycle-regulated promoters that are affected by this pathway, providing an explanation of how (p)ppGpp-signaling might couple starvation to control cell cycle progression in Caulobacter spp. and likely other Alphaproteobacteria. This pathway has the potential to integrate carbon fluctuation into cell cycle control, since in phosphotransferase systems it is the glycolytic product phosphenolpyruvate (PEP) rather than ATP that is used as the phosphor donor for phosphorylation.Stefano SanselicioPatrick H. ViollierAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 5 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Stefano Sanselicio Patrick H. Viollier Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains
description	ABSTRACT Despite the myriad of different sensory domains encoded in bacterial genomes, only a few are known to control the cell cycle. Here, suppressor genetics was used to unveil the regulatory interplay between the PAS (Per-Arnt-Sim) domain protein MopJ and the uncharacterized GAF (cyclic GMP-phosphodiesterase–adenylyl cyclase–FhlA) domain protein PtsP, which resembles an alternative component of the phosphoenolpyruvate (PEP) transferase system. Both of these systems indirectly target the Caulobacter crescentus cell cycle master regulator CtrA, but in different ways. While MopJ acts on CtrA via the cell cycle kinases DivJ and DivL, which control the removal of CtrA at the G1-S transition, our data show that PtsP signals through the conserved alarmone (p)ppGpp, which prevents CtrA cycling under nutritional stress and in stationary phase. We found that PtsP interacts genetically and physically with the (p)ppGpp synthase/hydrolase SpoT and that it modulates several promoters that are directly activated by the cell cycle transcriptional regulator GcrA. Thus, parallel systems integrate nutritional and systemic signals within the cell cycle transcriptional network, converging on the essential alphaproteobacterial regulator CtrA while also affecting global cell cycle transcription in other ways. IMPORTANCE Many alphaproteobacteria divide asymmetrically, and their cell cycle progression is carefully regulated. How these bacteria control the cell cycle in response to nutrient limitation is not well understood. Here, we identify a multicomponent signaling pathway that acts on the cell cycle when nutrients become scarce in stationary phase. We show that efficient accumulation of the master cell cycle regulator CtrA in stationary-phase Caulobacter crescentus cells requires the previously identified stationary-phase/cell cycle regulator MopJ as well as the phosphoenolpyruvate protein phosphotransferase PtsP, which acts via the conserved (p)ppGpp synthase SpoT. We identify cell cycle-regulated promoters that are affected by this pathway, providing an explanation of how (p)ppGpp-signaling might couple starvation to control cell cycle progression in Caulobacter spp. and likely other Alphaproteobacteria. This pathway has the potential to integrate carbon fluctuation into cell cycle control, since in phosphotransferase systems it is the glycolytic product phosphenolpyruvate (PEP) rather than ATP that is used as the phosphor donor for phosphorylation.
format	article
author	Stefano Sanselicio Patrick H. Viollier
author_facet	Stefano Sanselicio Patrick H. Viollier
author_sort	Stefano Sanselicio
title	Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains
title_short	Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains
title_full	Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains
title_fullStr	Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains
title_full_unstemmed	Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains
title_sort	convergence of alarmone and cell cycle signaling from <italic toggle="yes">trans</italic>-encoded sensory domains
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/7df787c9ce1848b6ad679a40879e22b0
work_keys_str_mv	AT stefanosanselicio convergenceofalarmoneandcellcyclesignalingfromitalictoggleyestransitalicencodedsensorydomains AT patrickhviollier convergenceofalarmoneandcellcyclesignalingfromitalictoggleyestransitalicencodedsensorydomains
_version_	1718427713973256192

Convergence of Alarmone and Cell Cycle Signaling from <italic toggle="yes">Trans</italic>-Encoded Sensory Domains

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