Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.

Transcriptional regulation by binding of transcription factors to palindromic sequences in promoter regions is a fundamental process in bacteria. Some transcription factors have multiple dimeric DNA-binding domains, in principle enabling interaction with higher-order DNA structures; however, mechani...

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Main Authors: Frederik Oskar Graversgaard Henriksen, Lan Bich Van, Ditlev Egeskov Brodersen, Ragnhild Bager Skjerning
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-06-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011749
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author Frederik Oskar Graversgaard Henriksen
Lan Bich Van
Ditlev Egeskov Brodersen
Ragnhild Bager Skjerning
author_facet Frederik Oskar Graversgaard Henriksen
Lan Bich Van
Ditlev Egeskov Brodersen
Ragnhild Bager Skjerning
author_sort Frederik Oskar Graversgaard Henriksen
collection DOAJ
description Transcriptional regulation by binding of transcription factors to palindromic sequences in promoter regions is a fundamental process in bacteria. Some transcription factors have multiple dimeric DNA-binding domains, in principle enabling interaction with higher-order DNA structures; however, mechanistic and structural insights into this phenomenon remain limited. The Pseudomonas putida toxin-antitoxin (TA) system Xre-RES has an unusual 4:2 stoichiometry including two potential DNA-binding sites, compatible with a complex mechanism of transcriptional autoregulation. Here, we show that the Xre-RES complex interacts specifically with a palindromic DNA repeat in the promoter in a 1:1 molar ratio, leading to transcriptional repression. We determine the 2.7 Å crystal structure of the protein-DNA complex, revealing an unexpected asymmetry in the interaction and suggesting the presence of a secondary binding site, which is supported by structural prediction of the binding to the intact promoter region. Additionally, we show that the antitoxin can be partially dislodged from the Xre-RES complex, resulting in Xre monomers and a 2:2 Xre-RES complex, neither of which repress transcription. These findings highlight a dynamic, concentration-dependent model of transcriptional autoregulation, in which the Xre-RES complex transitions between a non-binding (2:2) and a DNA-binding (4:2) form.
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spelling doaj-art-dacef08bc05d4208a929256c423b63b52025-08-23T05:31:37ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042025-06-01216e101174910.1371/journal.pgen.1011749Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.Frederik Oskar Graversgaard HenriksenLan Bich VanDitlev Egeskov BrodersenRagnhild Bager SkjerningTranscriptional regulation by binding of transcription factors to palindromic sequences in promoter regions is a fundamental process in bacteria. Some transcription factors have multiple dimeric DNA-binding domains, in principle enabling interaction with higher-order DNA structures; however, mechanistic and structural insights into this phenomenon remain limited. The Pseudomonas putida toxin-antitoxin (TA) system Xre-RES has an unusual 4:2 stoichiometry including two potential DNA-binding sites, compatible with a complex mechanism of transcriptional autoregulation. Here, we show that the Xre-RES complex interacts specifically with a palindromic DNA repeat in the promoter in a 1:1 molar ratio, leading to transcriptional repression. We determine the 2.7 Å crystal structure of the protein-DNA complex, revealing an unexpected asymmetry in the interaction and suggesting the presence of a secondary binding site, which is supported by structural prediction of the binding to the intact promoter region. Additionally, we show that the antitoxin can be partially dislodged from the Xre-RES complex, resulting in Xre monomers and a 2:2 Xre-RES complex, neither of which repress transcription. These findings highlight a dynamic, concentration-dependent model of transcriptional autoregulation, in which the Xre-RES complex transitions between a non-binding (2:2) and a DNA-binding (4:2) form.https://doi.org/10.1371/journal.pgen.1011749
spellingShingle Frederik Oskar Graversgaard Henriksen
Lan Bich Van
Ditlev Egeskov Brodersen
Ragnhild Bager Skjerning
Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.
PLoS Genetics
title Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.
title_full Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.
title_fullStr Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.
title_full_unstemmed Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.
title_short Structural basis for higher-order DNA binding by a bacterial transcriptional regulator.
title_sort structural basis for higher order dna binding by a bacterial transcriptional regulator
url https://doi.org/10.1371/journal.pgen.1011749
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