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An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica

Bacteria acquire P primarily as inorganic orthophosphate (Pi, PO(4)(3−)). Once internalized, Pi is rapidly assimilated into biomass during the synthesis of ATP. Because Pi is essential, but excessive ATP is toxic, the acquisition of environmental Pi is tightly regulated. In the bacterium Salmonella...

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Autores principales: Bruna, Roberto E., Kendra, Christopher G., Pontes, Mauricio H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10055408/
https://www.ncbi.nlm.nih.gov/pubmed/36993483
http://dx.doi.org/10.1101/2023.03.23.533958
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author Bruna, Roberto E.
Kendra, Christopher G.
Pontes, Mauricio H.
author_facet Bruna, Roberto E.
Kendra, Christopher G.
Pontes, Mauricio H.
author_sort Bruna, Roberto E.
collection PubMed
description Bacteria acquire P primarily as inorganic orthophosphate (Pi, PO(4)(3−)). Once internalized, Pi is rapidly assimilated into biomass during the synthesis of ATP. Because Pi is essential, but excessive ATP is toxic, the acquisition of environmental Pi is tightly regulated. In the bacterium Salmonella enterica (Salmonella), growth in Pi-limiting environments activates the membrane sensor histidine kinase PhoR, leading to the phosphorylation of its cognate transcriptional regulator PhoB and subsequent transcription of genes involved in adaptations to low Pi. Pi limitation is thought to promote PhoR kinase activity by altering the conformation of a membrane signaling complex comprised by PhoR, the multicomponent Pi transporter system PstSACB and the regulatory protein PhoU. However, the identity of the low Pi signal and how it controls PhoR activity remain unknown. Here we characterize the PhoB-dependent and independent transcriptional changes elicited by Salmonella in response to P starvation, and identify PhoB-independent genes that are required for the utilization of several organic-P sources. We use this knowledge to identify the cellular compartment where the PhoR signaling complex senses the Pi-limiting signal. We demonstrate that the PhoB and PhoR signal transduction proteins can be maintained in an inactive state even when Salmonella is grown in media lacking Pi. Our results establish that PhoR activity is controlled by an intracellular signal resulting from P insufficiency.
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spelling pubmed-100554082023-03-30 An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica Bruna, Roberto E. Kendra, Christopher G. Pontes, Mauricio H. bioRxiv Article Bacteria acquire P primarily as inorganic orthophosphate (Pi, PO(4)(3−)). Once internalized, Pi is rapidly assimilated into biomass during the synthesis of ATP. Because Pi is essential, but excessive ATP is toxic, the acquisition of environmental Pi is tightly regulated. In the bacterium Salmonella enterica (Salmonella), growth in Pi-limiting environments activates the membrane sensor histidine kinase PhoR, leading to the phosphorylation of its cognate transcriptional regulator PhoB and subsequent transcription of genes involved in adaptations to low Pi. Pi limitation is thought to promote PhoR kinase activity by altering the conformation of a membrane signaling complex comprised by PhoR, the multicomponent Pi transporter system PstSACB and the regulatory protein PhoU. However, the identity of the low Pi signal and how it controls PhoR activity remain unknown. Here we characterize the PhoB-dependent and independent transcriptional changes elicited by Salmonella in response to P starvation, and identify PhoB-independent genes that are required for the utilization of several organic-P sources. We use this knowledge to identify the cellular compartment where the PhoR signaling complex senses the Pi-limiting signal. We demonstrate that the PhoB and PhoR signal transduction proteins can be maintained in an inactive state even when Salmonella is grown in media lacking Pi. Our results establish that PhoR activity is controlled by an intracellular signal resulting from P insufficiency. Cold Spring Harbor Laboratory 2023-03-23 /pmc/articles/PMC10055408/ /pubmed/36993483 http://dx.doi.org/10.1101/2023.03.23.533958 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Bruna, Roberto E.
Kendra, Christopher G.
Pontes, Mauricio H.
An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica
title An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica
title_full An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica
title_fullStr An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica
title_full_unstemmed An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica
title_short An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in Salmonella enterica
title_sort intracellular phosphorus-starvation signal activates the phob/phor two-component system in salmonella enterica
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10055408/
https://www.ncbi.nlm.nih.gov/pubmed/36993483
http://dx.doi.org/10.1101/2023.03.23.533958
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