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Single-molecule imaging of DNA gyrase activity in living Escherichia coli

Bacterial DNA gyrase introduces negative supercoils into chromosomal DNA and relaxes positive supercoils introduced by replication and transiently by transcription. Removal of these positive supercoils is essential for replication fork progression and for the overall unlinking of the two duplex DNA...

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Autores principales: Stracy, Mathew, Wollman, Adam J M, Kaja, Elzbieta, Gapinski, Jacek, Lee, Ji-Eun, Leek, Victoria A, McKie, Shannon J, Mitchenall, Lesley A, Maxwell, Anthony, Sherratt, David J, Leake, Mark C, Zawadzki, Pawel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6326794/
https://www.ncbi.nlm.nih.gov/pubmed/30445553
http://dx.doi.org/10.1093/nar/gky1143
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author Stracy, Mathew
Wollman, Adam J M
Kaja, Elzbieta
Gapinski, Jacek
Lee, Ji-Eun
Leek, Victoria A
McKie, Shannon J
Mitchenall, Lesley A
Maxwell, Anthony
Sherratt, David J
Leake, Mark C
Zawadzki, Pawel
author_facet Stracy, Mathew
Wollman, Adam J M
Kaja, Elzbieta
Gapinski, Jacek
Lee, Ji-Eun
Leek, Victoria A
McKie, Shannon J
Mitchenall, Lesley A
Maxwell, Anthony
Sherratt, David J
Leake, Mark C
Zawadzki, Pawel
author_sort Stracy, Mathew
collection PubMed
description Bacterial DNA gyrase introduces negative supercoils into chromosomal DNA and relaxes positive supercoils introduced by replication and transiently by transcription. Removal of these positive supercoils is essential for replication fork progression and for the overall unlinking of the two duplex DNA strands, as well as for ongoing transcription. To address how gyrase copes with these topological challenges, we used high-speed single-molecule fluorescence imaging in live Escherichia coli cells. We demonstrate that at least 300 gyrase molecules are stably bound to the chromosome at any time, with ∼12 enzymes enriched near each replication fork. Trapping of reaction intermediates with ciprofloxacin revealed complexes undergoing catalysis. Dwell times of ∼2 s were observed for the dispersed gyrase molecules, which we propose maintain steady-state levels of negative supercoiling of the chromosome. In contrast, the dwell time of replisome-proximal molecules was ∼8 s, consistent with these catalyzing processive positive supercoil relaxation in front of the progressing replisome.
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spelling pubmed-63267942019-01-15 Single-molecule imaging of DNA gyrase activity in living Escherichia coli Stracy, Mathew Wollman, Adam J M Kaja, Elzbieta Gapinski, Jacek Lee, Ji-Eun Leek, Victoria A McKie, Shannon J Mitchenall, Lesley A Maxwell, Anthony Sherratt, David J Leake, Mark C Zawadzki, Pawel Nucleic Acids Res Genome Integrity, Repair and Replication Bacterial DNA gyrase introduces negative supercoils into chromosomal DNA and relaxes positive supercoils introduced by replication and transiently by transcription. Removal of these positive supercoils is essential for replication fork progression and for the overall unlinking of the two duplex DNA strands, as well as for ongoing transcription. To address how gyrase copes with these topological challenges, we used high-speed single-molecule fluorescence imaging in live Escherichia coli cells. We demonstrate that at least 300 gyrase molecules are stably bound to the chromosome at any time, with ∼12 enzymes enriched near each replication fork. Trapping of reaction intermediates with ciprofloxacin revealed complexes undergoing catalysis. Dwell times of ∼2 s were observed for the dispersed gyrase molecules, which we propose maintain steady-state levels of negative supercoiling of the chromosome. In contrast, the dwell time of replisome-proximal molecules was ∼8 s, consistent with these catalyzing processive positive supercoil relaxation in front of the progressing replisome. Oxford University Press 2019-01-10 2018-11-16 /pmc/articles/PMC6326794/ /pubmed/30445553 http://dx.doi.org/10.1093/nar/gky1143 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Genome Integrity, Repair and Replication
Stracy, Mathew
Wollman, Adam J M
Kaja, Elzbieta
Gapinski, Jacek
Lee, Ji-Eun
Leek, Victoria A
McKie, Shannon J
Mitchenall, Lesley A
Maxwell, Anthony
Sherratt, David J
Leake, Mark C
Zawadzki, Pawel
Single-molecule imaging of DNA gyrase activity in living Escherichia coli
title Single-molecule imaging of DNA gyrase activity in living Escherichia coli
title_full Single-molecule imaging of DNA gyrase activity in living Escherichia coli
title_fullStr Single-molecule imaging of DNA gyrase activity in living Escherichia coli
title_full_unstemmed Single-molecule imaging of DNA gyrase activity in living Escherichia coli
title_short Single-molecule imaging of DNA gyrase activity in living Escherichia coli
title_sort single-molecule imaging of dna gyrase activity in living escherichia coli
topic Genome Integrity, Repair and Replication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6326794/
https://www.ncbi.nlm.nih.gov/pubmed/30445553
http://dx.doi.org/10.1093/nar/gky1143
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