Function of Nucleoid-Associated Proteins in Chromosome Structuring and Transcriptional Regulation

Dorman, Charles J.

doi:10.1159/000368850

Cited by 58 publications

(49 citation statements)

References 217 publications

(248 reference statements)

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“…In contrast, DNA in vivo is highly organized and condensed. In bacteria, this condensation is caused by nucleoid-associated proteins (NAPs) that collectively shape the chromosome (2,3). NAPs are capable of binding genomic DNA and in doing so alter its shape, control the transcriptional expression of genes, and remodel the structure of the nucleoid in response to external stimuli (2,3).…”

mentioning

confidence: 99%

Hysteresis in DNA compaction by Dps is described by an Ising model

Vtyurina

Dulin

Docter

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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In all organisms, DNA molecules are tightly compacted into a dynamic 3D nucleoprotein complex. In bacteria, this compaction is governed by the family of nucleoid-associated proteins (NAPs). Under conditions of stress and starvation, an NAP called Dps (DNAbinding protein from starved cells) becomes highly up-regulated and can massively reorganize the bacterial chromosome. Although static structures of Dps-DNA complexes have been documented, little is known about the dynamics of their assembly. Here, we use fluorescence microscopy and magnetic-tweezers measurements to resolve the process of DNA compaction by Dps. Real-time in vitro studies demonstrated a highly cooperative process of Dps binding characterized by an abrupt collapse of the DNA extension, even under applied tension. Surprisingly, we also discovered a reproducible hysteresis in the process of compaction and decompaction of the Dps-DNA complex. This hysteresis is extremely stable over hour-long timescales despite the rapid binding and dissociation rates of Dps. A modified Ising model is successfully applied to fit these kinetic features. We find that long-lived hysteresis arises naturally as a consequence of protein cooperativity in large complexes and provides a useful mechanism for cells to adopt unique epigenetic states.DNA condensation | Dps | cooperativity | hysteresis | Ising model P urified DNA behaves as an entropic spring with a radius of gyration that scales as a function of the contour length (1). In contrast, DNA in vivo is highly organized and condensed. In bacteria, this condensation is caused by nucleoid-associated proteins (NAPs) that collectively shape the chromosome (2, 3). NAPs are capable of binding genomic DNA and in doing so alter its shape, control the transcriptional expression of genes, and remodel the structure of the nucleoid in response to external stimuli (2, 3).DNA-binding protein from starved cells (Dps) is an NAP structurally related to ferritins and associated with the response to stress. Dps is highly expressed in stationary phase (4-7) and is also involved in the cellular response to oxidative (4, 8-10), UV (8, 11), thermal (8), and pH shocks (8). In addition, Dps has been implicated in biofilm formation and tolerance to bacteriophage attacks (12). Dps monomers have a molecular mass of 19 kDa and assemble into a dodecameric shell (Fig. S1A) (13). The resulting complex binds to both supercoiled and linear DNA to form a dense biocrystal structure (4,7,9,14).Although the crystal structure of the Dps dodecamer has been solved (13), no atomic-scale structure of Dps-DNA assemblies currently exists and little is known about complex formation. The affinity of Dps for DNA is very sensitive to buffer conditions. Like many DNA-binding proteins, Dps binds DNA more weakly in the presence of higher salt concentrations. Less typically, divalent cations such as Mg 2+ can substantially weaken the affinity of Dps for DNA (9, 15). It has been proposed that fluctuations in divalent cation concentrations act as a trigger for biocrystal as...

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mentioning

confidence: 99%

Hysteresis in DNA compaction by Dps is described by an Ising model

Vtyurina

Dulin

Docter

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…As such, much attention has been devoted to the study of the functional properties of the nucleoid as well as its interactions with associated proteins (Dillon and Dorman, 2010; Dorman, 2014). Less is known about the global and domain-level structure dynamics of the nucleoid, and it is often stated in general literature that there is no major organization of the hereditary material in prokaryotes (Reece and Urry, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…In general, the NAPs are highly conserved within specific bacterial families, but a few are highly conserved among all prokaryotic species, suggesting a fundamental advantage of nucleoid structuring that has been further improved in the course of evolution. All bacterial species encode at least one NAP (Dorman, 2014). …”

Section: The Living Nucleoidmentioning

confidence: 99%

“…H-NS binding has been proposed as a mechanism for avoiding the unwanted expression of newly acquired genes that have yet to be integrated into existing cellular processes (Doyle et al, 2007; Paytubi et al, 2013; Dorman, 2014). This makes it possible for bacteria to obtain e.g., large pathogenicity islands that would otherwise represent a massive burden.…”

Section: The Evolving Nucleoidmentioning

confidence: 99%

“…Evidence of supercoiling release has been observed at specific REP elements located at the end of certain open reading frames. REP elements are recognized by the DNA gyrase to enable quick relief of the positive supercoil introduced by RNAP (Dorman, 2014). Barriers restricting the transmission of DNA supercoiling can be formed by binding of NAPs (Rogozin et al, 2002; Meyer and Beslon, 2014).…”

Section: The Evolving Nucleoidmentioning

confidence: 99%

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Impact of Chromosomal Architecture on the Function and Evolution of Bacterial Genomes

2018

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The bacterial nucleoid is highly condensed and forms compartment-like structures within the cell. Much attention has been devoted to investigating the dynamic topology and organization of the nucleoid. In contrast, the specific nucleoid organization, and the relationship between nucleoid structure and function is often neglected with regard to importance for adaption to changing environments and horizontal gene acquisition. In this review, we focus on the structure-function relationship in the bacterial nucleoid. We provide an overview of the fundamental properties that shape the chromosome as a structured yet dynamic macromolecule. These fundamental properties are then considered in the context of the living cell, with focus on how the informational flow affects the nucleoid structure, which in turn impacts on the genetic output. Subsequently, the dynamic living nucleoid will be discussed in the context of evolution. We will address how the acquisition of foreign DNA impacts nucleoid structure, and conversely, how nucleoid structure constrains the successful and sustainable chromosomal integration of novel DNA. Finally, we will discuss current challenges and directions of research in understanding the role of chromosomal architecture in bacterial survival and adaptation.

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2020

Structure and Function of the Bacterial Genome

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Function of Nucleoid-Associated Proteins in Chromosome Structuring and Transcriptional Regulation

Cited by 58 publications

References 217 publications

Hysteresis in DNA compaction by Dps is described by an Ising model

Hysteresis in DNA compaction by Dps is described by an Ising model

Impact of Chromosomal Architecture on the Function and Evolution of Bacterial Genomes

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