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The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner
Dps is a multifunctional homododecameric protein that oxidizes Fe(2+) ions accumulating them in the form of Fe(2)O(3) within its protein cavity, interacts with DNA tightly condensing bacterial nucleoid upon starvation and performs some other functions. During the last two decades from discovery of t...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5553809/ https://www.ncbi.nlm.nih.gov/pubmed/28800583 http://dx.doi.org/10.1371/journal.pone.0182800 |
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author | Antipov, S. S. Tutukina, M. N. Preobrazhenskaya, E. V. Kondrashov, F. A. Patrushev, M. V. Toshchakov, S. V. Dominova, I. Shvyreva, U. S. Vrublevskaya, V. V. Morenkov, O. S. Sukharicheva, N. A. Panyukov, V. V. Ozoline, O. N. |
author_facet | Antipov, S. S. Tutukina, M. N. Preobrazhenskaya, E. V. Kondrashov, F. A. Patrushev, M. V. Toshchakov, S. V. Dominova, I. Shvyreva, U. S. Vrublevskaya, V. V. Morenkov, O. S. Sukharicheva, N. A. Panyukov, V. V. Ozoline, O. N. |
author_sort | Antipov, S. S. |
collection | PubMed |
description | Dps is a multifunctional homododecameric protein that oxidizes Fe(2+) ions accumulating them in the form of Fe(2)O(3) within its protein cavity, interacts with DNA tightly condensing bacterial nucleoid upon starvation and performs some other functions. During the last two decades from discovery of this protein, its ferroxidase activity became rather well studied, but the mechanism of Dps interaction with DNA still remains enigmatic. The crucial role of lysine residues in the unstructured N-terminal tails led to the conventional point of view that Dps binds DNA without sequence or structural specificity. However, deletion of dps changed the profile of proteins in starved cells, SELEX screen revealed genomic regions preferentially bound in vitro and certain affinity of Dps for artificial branched molecules was detected by atomic force microscopy. Here we report a non-random distribution of Dps binding sites across the bacterial chromosome in exponentially growing cells and show their enrichment with inverted repeats prone to form secondary structures. We found that the Dps-bound regions overlap with sites occupied by other nucleoid proteins, and contain overrepresented motifs typical for their consensus sequences. Of the two types of genomic domains with extensive protein occupancy, which can be highly expressed or transcriptionally silent only those that are enriched with RNA polymerase molecules were preferentially occupied by Dps. In the dps-null mutant we, therefore, observed a differentially altered expression of several targeted genes and found suppressed transcription from the dps promoter. In most cases this can be explained by the relieved interference with Dps for nucleoid proteins exploiting sequence-specific modes of DNA binding. Thus, protecting bacterial cells from different stresses during exponential growth, Dps can modulate transcriptional integrity of the bacterial chromosome hampering RNA biosynthesis from some genes via competition with RNA polymerase or, vice versa, competing with inhibitors to activate transcription. |
format | Online Article Text |
id | pubmed-5553809 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-55538092017-08-25 The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner Antipov, S. S. Tutukina, M. N. Preobrazhenskaya, E. V. Kondrashov, F. A. Patrushev, M. V. Toshchakov, S. V. Dominova, I. Shvyreva, U. S. Vrublevskaya, V. V. Morenkov, O. S. Sukharicheva, N. A. Panyukov, V. V. Ozoline, O. N. PLoS One Research Article Dps is a multifunctional homododecameric protein that oxidizes Fe(2+) ions accumulating them in the form of Fe(2)O(3) within its protein cavity, interacts with DNA tightly condensing bacterial nucleoid upon starvation and performs some other functions. During the last two decades from discovery of this protein, its ferroxidase activity became rather well studied, but the mechanism of Dps interaction with DNA still remains enigmatic. The crucial role of lysine residues in the unstructured N-terminal tails led to the conventional point of view that Dps binds DNA without sequence or structural specificity. However, deletion of dps changed the profile of proteins in starved cells, SELEX screen revealed genomic regions preferentially bound in vitro and certain affinity of Dps for artificial branched molecules was detected by atomic force microscopy. Here we report a non-random distribution of Dps binding sites across the bacterial chromosome in exponentially growing cells and show their enrichment with inverted repeats prone to form secondary structures. We found that the Dps-bound regions overlap with sites occupied by other nucleoid proteins, and contain overrepresented motifs typical for their consensus sequences. Of the two types of genomic domains with extensive protein occupancy, which can be highly expressed or transcriptionally silent only those that are enriched with RNA polymerase molecules were preferentially occupied by Dps. In the dps-null mutant we, therefore, observed a differentially altered expression of several targeted genes and found suppressed transcription from the dps promoter. In most cases this can be explained by the relieved interference with Dps for nucleoid proteins exploiting sequence-specific modes of DNA binding. Thus, protecting bacterial cells from different stresses during exponential growth, Dps can modulate transcriptional integrity of the bacterial chromosome hampering RNA biosynthesis from some genes via competition with RNA polymerase or, vice versa, competing with inhibitors to activate transcription. Public Library of Science 2017-08-11 /pmc/articles/PMC5553809/ /pubmed/28800583 http://dx.doi.org/10.1371/journal.pone.0182800 Text en © 2017 Antipov et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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 Antipov, S. S. Tutukina, M. N. Preobrazhenskaya, E. V. Kondrashov, F. A. Patrushev, M. V. Toshchakov, S. V. Dominova, I. Shvyreva, U. S. Vrublevskaya, V. V. Morenkov, O. S. Sukharicheva, N. A. Panyukov, V. V. Ozoline, O. N. The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner |
title | The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner |
title_full | The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner |
title_fullStr | The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner |
title_full_unstemmed | The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner |
title_short | The nucleoid protein Dps binds genomic DNA of Escherichia coli in a non-random manner |
title_sort | nucleoid protein dps binds genomic dna of escherichia coli in a non-random manner |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5553809/ https://www.ncbi.nlm.nih.gov/pubmed/28800583 http://dx.doi.org/10.1371/journal.pone.0182800 |
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