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Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth

Bacterial chromosome topology is controlled by topoisomerases and nucleoid-associated proteins (NAPs). While topoisomerases regulate DNA supercoiling, NAPs introduce bends or coat DNA upon its binding, affecting DNA loop formation. Streptomyces, hyphal, multigenomic bacteria known for producing nume...

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Autores principales: Strzałka, Agnieszka, Kois-Ostrowska, Agnieszka, Kędra, Magda, Łebkowski, Tomasz, Bieniarz, Grażyna, Szafran, Marcin J, Jakimowicz, Dagmara
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9756944/
https://www.ncbi.nlm.nih.gov/pubmed/36420903
http://dx.doi.org/10.1093/nar/gkac1093
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author Strzałka, Agnieszka
Kois-Ostrowska, Agnieszka
Kędra, Magda
Łebkowski, Tomasz
Bieniarz, Grażyna
Szafran, Marcin J
Jakimowicz, Dagmara
author_facet Strzałka, Agnieszka
Kois-Ostrowska, Agnieszka
Kędra, Magda
Łebkowski, Tomasz
Bieniarz, Grażyna
Szafran, Marcin J
Jakimowicz, Dagmara
author_sort Strzałka, Agnieszka
collection PubMed
description Bacterial chromosome topology is controlled by topoisomerases and nucleoid-associated proteins (NAPs). While topoisomerases regulate DNA supercoiling, NAPs introduce bends or coat DNA upon its binding, affecting DNA loop formation. Streptomyces, hyphal, multigenomic bacteria known for producing numerous clinically important compounds, use the highly processive topoisomerase I (TopA) to remove excessive negative DNA supercoils. Elongated vegetative Streptomyces cells contain multiple copies of their linear chromosome, which remain relaxed and relatively evenly distributed. Here, we explored how TopA cooperates with HupA, an HU homologue that is the most abundant Streptomyces NAP. We verified that HupA has an increased affinity for supercoiled DNA in vivo and in vitro. Analysis of mutant strains demonstrated that HupA elimination is detrimental under high DNA supercoiling conditions. The absence of HupA, combined with decreased TopA levels, disrupted chromosome distribution in hyphal cells, eventually inhibiting hyphal growth. We concluded that increased HupA binding to DNA under elevated chromosome supercoiling conditions is critical for the preservation of chromosome organisation.
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spelling pubmed-97569442022-12-16 Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth Strzałka, Agnieszka Kois-Ostrowska, Agnieszka Kędra, Magda Łebkowski, Tomasz Bieniarz, Grażyna Szafran, Marcin J Jakimowicz, Dagmara Nucleic Acids Res Gene regulation, Chromatin and Epigenetics Bacterial chromosome topology is controlled by topoisomerases and nucleoid-associated proteins (NAPs). While topoisomerases regulate DNA supercoiling, NAPs introduce bends or coat DNA upon its binding, affecting DNA loop formation. Streptomyces, hyphal, multigenomic bacteria known for producing numerous clinically important compounds, use the highly processive topoisomerase I (TopA) to remove excessive negative DNA supercoils. Elongated vegetative Streptomyces cells contain multiple copies of their linear chromosome, which remain relaxed and relatively evenly distributed. Here, we explored how TopA cooperates with HupA, an HU homologue that is the most abundant Streptomyces NAP. We verified that HupA has an increased affinity for supercoiled DNA in vivo and in vitro. Analysis of mutant strains demonstrated that HupA elimination is detrimental under high DNA supercoiling conditions. The absence of HupA, combined with decreased TopA levels, disrupted chromosome distribution in hyphal cells, eventually inhibiting hyphal growth. We concluded that increased HupA binding to DNA under elevated chromosome supercoiling conditions is critical for the preservation of chromosome organisation. Oxford University Press 2022-11-24 /pmc/articles/PMC9756944/ /pubmed/36420903 http://dx.doi.org/10.1093/nar/gkac1093 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Gene regulation, Chromatin and Epigenetics
Strzałka, Agnieszka
Kois-Ostrowska, Agnieszka
Kędra, Magda
Łebkowski, Tomasz
Bieniarz, Grażyna
Szafran, Marcin J
Jakimowicz, Dagmara
Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth
title Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth
title_full Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth
title_fullStr Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth
title_full_unstemmed Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth
title_short Enhanced binding of an HU homologue under increased DNA supercoiling preserves chromosome organisation and sustains Streptomyces hyphal growth
title_sort enhanced binding of an hu homologue under increased dna supercoiling preserves chromosome organisation and sustains streptomyces hyphal growth
topic Gene regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9756944/
https://www.ncbi.nlm.nih.gov/pubmed/36420903
http://dx.doi.org/10.1093/nar/gkac1093
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