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A cryptic transcription factor regulates Caulobacter adhesin development

Alphaproteobacteria commonly produce an adhesin that is anchored to the exterior of the envelope at one cell pole. In Caulobacter crescentus this adhesin, known as the holdfast, facilitates attachment to solid surfaces and cell partitioning to air-liquid interfaces. An ensemble of two-component sign...

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Autores principales: McLaughlin, Maeve, Hershey, David M., Reyes Ruiz, Leila M., Fiebig, Aretha, Crosson, Sean
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9648850/
https://www.ncbi.nlm.nih.gov/pubmed/36315598
http://dx.doi.org/10.1371/journal.pgen.1010481
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author McLaughlin, Maeve
Hershey, David M.
Reyes Ruiz, Leila M.
Fiebig, Aretha
Crosson, Sean
author_facet McLaughlin, Maeve
Hershey, David M.
Reyes Ruiz, Leila M.
Fiebig, Aretha
Crosson, Sean
author_sort McLaughlin, Maeve
collection PubMed
description Alphaproteobacteria commonly produce an adhesin that is anchored to the exterior of the envelope at one cell pole. In Caulobacter crescentus this adhesin, known as the holdfast, facilitates attachment to solid surfaces and cell partitioning to air-liquid interfaces. An ensemble of two-component signal transduction (TCS) proteins controls C. crescentus holdfast biogenesis by indirectly regulating expression of HfiA, a potent inhibitor of holdfast synthesis. We performed a genetic selection to discover direct hfiA regulators that function downstream of the adhesion TCS system and identified rtrC, a hypothetical gene. rtrC transcription is directly activated by the adhesion TCS regulator, SpdR. Though its primary structure bears no resemblance to any defined protein family, RtrC binds and regulates dozens of sites on the C. crescentus chromosome via a pseudo-palindromic sequence. Among these binding sites is the hfiA promoter, where RtrC functions to directly repress transcription and thereby activate holdfast development. Either RtrC or SpdR can directly activate transcription of a second hfiA repressor, rtrB. Thus, environmental regulation of hfiA transcription by the adhesion TCS system is subject to control by an OR-gated type I coherent feedforward loop; these regulatory motifs are known to buffer gene expression against fluctuations in regulating signals. We have further assessed the functional role of rtrC in holdfast-dependent processes, including surface adherence to a cellulosic substrate and formation of pellicle biofilms at air-liquid interfaces. Strains harboring insertional mutations in rtrC have a diminished adhesion profile in a competitive cheesecloth binding assay and a reduced capacity to colonize pellicle biofilms in select media conditions. Our results add to an emerging understanding of the regulatory topology and molecular components of a complex bacterial cell adhesion control system.
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spelling pubmed-96488502022-11-15 A cryptic transcription factor regulates Caulobacter adhesin development McLaughlin, Maeve Hershey, David M. Reyes Ruiz, Leila M. Fiebig, Aretha Crosson, Sean PLoS Genet Research Article Alphaproteobacteria commonly produce an adhesin that is anchored to the exterior of the envelope at one cell pole. In Caulobacter crescentus this adhesin, known as the holdfast, facilitates attachment to solid surfaces and cell partitioning to air-liquid interfaces. An ensemble of two-component signal transduction (TCS) proteins controls C. crescentus holdfast biogenesis by indirectly regulating expression of HfiA, a potent inhibitor of holdfast synthesis. We performed a genetic selection to discover direct hfiA regulators that function downstream of the adhesion TCS system and identified rtrC, a hypothetical gene. rtrC transcription is directly activated by the adhesion TCS regulator, SpdR. Though its primary structure bears no resemblance to any defined protein family, RtrC binds and regulates dozens of sites on the C. crescentus chromosome via a pseudo-palindromic sequence. Among these binding sites is the hfiA promoter, where RtrC functions to directly repress transcription and thereby activate holdfast development. Either RtrC or SpdR can directly activate transcription of a second hfiA repressor, rtrB. Thus, environmental regulation of hfiA transcription by the adhesion TCS system is subject to control by an OR-gated type I coherent feedforward loop; these regulatory motifs are known to buffer gene expression against fluctuations in regulating signals. We have further assessed the functional role of rtrC in holdfast-dependent processes, including surface adherence to a cellulosic substrate and formation of pellicle biofilms at air-liquid interfaces. Strains harboring insertional mutations in rtrC have a diminished adhesion profile in a competitive cheesecloth binding assay and a reduced capacity to colonize pellicle biofilms in select media conditions. Our results add to an emerging understanding of the regulatory topology and molecular components of a complex bacterial cell adhesion control system. Public Library of Science 2022-10-31 /pmc/articles/PMC9648850/ /pubmed/36315598 http://dx.doi.org/10.1371/journal.pgen.1010481 Text en © 2022 McLaughlin et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
McLaughlin, Maeve
Hershey, David M.
Reyes Ruiz, Leila M.
Fiebig, Aretha
Crosson, Sean
A cryptic transcription factor regulates Caulobacter adhesin development
title A cryptic transcription factor regulates Caulobacter adhesin development
title_full A cryptic transcription factor regulates Caulobacter adhesin development
title_fullStr A cryptic transcription factor regulates Caulobacter adhesin development
title_full_unstemmed A cryptic transcription factor regulates Caulobacter adhesin development
title_short A cryptic transcription factor regulates Caulobacter adhesin development
title_sort cryptic transcription factor regulates caulobacter adhesin development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9648850/
https://www.ncbi.nlm.nih.gov/pubmed/36315598
http://dx.doi.org/10.1371/journal.pgen.1010481
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