Nucleoid-associated proteins shape chromatin structure and transcriptional regulation across the bacterial kingdom

Amemiya, Haley M.; Schroeder, Jeremy W.; Freddolino, Peter L.

doi:10.1080/21541264.2021.1973865

Cited by 51 publications

(51 citation statements)

References 349 publications

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“…Instead of having a membrane-bound nucleus similar to the nucleus of eukaryotes, bacteria pack their genomes into nucleoids through a series of nucleoid-associated proteins (NAPs) in distinct cytoplasmic regions. Differences in these NAPs are believed to form regions of chromatin, analogous to eukaryotic transcriptionally active heterochromatin and transcriptionally inactive euchromatin in bacteria [ 35 ]. Although it was previously claimed that bacteria do not possess histones and that bacterial epigenetics is limited to DNA methylation [ 20 , 36 ], there is now clear evidence that this is not the case.…”

Section: Overview Of Bacterial Epigeneticsmentioning

confidence: 99%

Epigenetic-Mediated Antimicrobial Resistance: Host versus Pathogen Epigenetic Alterations

et al. 2022

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Since the discovery of antibiotics, humans have been benefiting from them by decreasing the morbidity and mortality associated with bacterial infections. However, in the past few decades, misuse of antibiotics has led to the emergence of bacterial infections resistant to multiple drugs, a significant health concern. Bacteria exposed to inappropriate levels of antibiotics lead to several genetic changes, enabling them to survive in the host and become more resistant. Despite the understanding and targeting of genetic-based biochemical changes in the bacteria, the increasing levels of antibiotic resistance are not under control. Many reports hint at the role of epigenetic modifications in the bacterial genome and host epigenetic reprogramming due to interaction with resistant pathogens. Epigenetic changes, such as the DNA-methylation-based regulation of bacterial mutation rates or bacteria-induced histone modification in human epithelial cells, facilitate its long-term survival. In this review article, epigenetic changes leading to the development of antibiotic resistance in clinically relevant bacteria are discussed. Additionally, recent lines of evidence focusing on human host epigenetic changes due to the human–pathogen interactions are presented. As genetic mechanisms cannot explain the transient nature of antimicrobial resistance, we believe that epigenetics may provide new frontiers in antimicrobial discovery.

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Section: Overview Of Bacterial Epigeneticsmentioning

confidence: 99%

Epigenetic-Mediated Antimicrobial Resistance: Host versus Pathogen Epigenetic Alterations

et al. 2022

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“…Furthermore, the nucleoid was shown to undergo cycles of compaction-decompaction under the manipulation of crowding conditions [ 10 ], in line with the proposed switch-like conformational transition model for chromatin folding [ 11 ]. The regulatory role for “pre-programmed” phase transitions [ 9 ] was suggested by observations indicating that the nucleoid structure and gene expression are interdependent [ 6 , 12 , 13 , 14 , 15 , 16 ]. However, the tight coupling of chromosome structural transitions with gene expression dynamics appears at variance with the notion of gene expression as a fundamentally “noisy” stochastic process [ 17 ].…”

Section: Coupling Of Chromosomal Gene Order and Transcriptionmentioning

confidence: 99%

“…Thus, by operating with these two—discontinuous (digital) and continuous (analogue)—types of information interwoven in the very same genomic sequence, the DNA appears to communicate with itself. We propose that this “self-communication” represents the global feedback mechanism endowing the growing cell population with the capacity to monitor its status quo, a capacity that is reflected, in part, in the interdependence of chromosome structural dynamics and spatial patterns of gene expression [ 6 , 15 , 16 ].…”

Section: Coupling Of Dna Structure To Function Using Two Types Of Dna...mentioning

confidence: 99%

“…Conversely, on the transition to the stationary phase associated with the global relaxation of the DNA, the relatively A/T-rich Ter pole is activated, whereas the OriC pole is repressed. Since it is assumed, as mentioned above, that the chromosome configuration and genomic transcription are interdependent [ 6 , 15 , 16 , 119 , 120 ], the successive activation of OriC and Ter poles likely reflects the coordinately changing configuration and genetic activity of the chromosome, which is associated with the global redistribution of RNAP in the nucleoid [ 118 , 121 ]. In this regard, the non-random distribution of the binding sites of the NAPs and especially of the DNA gyrase and major RNAP sigma factors along the OriC-Ter axis that were observed in the E. coli genome [ 6 , 14 ], are suggestive.…”

Section: Role For Changing Chromosome Configuration In Organizing Gen...mentioning

confidence: 99%

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Spatiotemporal Coupling of DNA Supercoiling and Genomic Sequence Organization—A Timing Chain for the Bacterial Growth Cycle?

2022

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In this article we describe the bacterial growth cycle as a closed, self-reproducing, or autopoietic circuit, reestablishing the physiological state of stationary cells initially inoculated in the growth medium. In batch culture, this process of self-reproduction is associated with the gradual decline in available metabolic energy and corresponding change in the physiological state of the population as a function of “travelled distance” along the autopoietic path. We argue that this directional alteration of cell physiology is both reflected in and supported by sequential gene expression along the chromosomal OriC-Ter axis. We propose that during the E. coli growth cycle, the spatiotemporal order of gene expression is established by coupling the temporal gradient of supercoiling energy to the spatial gradient of DNA thermodynamic stability along the chromosomal OriC-Ter axis.

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“…NAPs can bind to DNA as monomers, dimers, or other organised structures [ 2 ]. H-NS, IHF, HU, Fis, and Dps are well-characterised NAPs of Escherichia coli and other species [ 3 ].…”

Section: Introductionmentioning

confidence: 99%

EbfC/YbaB: A Widely Distributed Nucleoid-Associated Protein in Prokaryotes

et al. 2022

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Genomic compaction is an essential characteristic of living organisms. Nucleoid-associated proteins (NAPs) are a group of small proteins that play crucial roles in chromosome architecture and affect DNA replication, transcription, and recombination by imposing topological alterations in genomic DNA, thereby modulating global gene expression. EbfC/YbaB was first described as a DNA-binding protein of Borrelia burgdorferi that regulates the expression of surface lipoproteins with roles in virulence. Further studies indicated that this protein binds specifically and non-specifically to DNA and colocalises with nucleoids in this bacterium. The data showed that this protein binds to DNA as a homodimer, although it can form other organised structures. Crystallography analysis indicated that the protein possesses domains responsible for protein–protein interactions and forms a “tweezer” structure probably involved in DNA binding. Moreover, sequence analysis revealed conserved motifs that may be associated with dimerisation. Structural analysis also showed that the tridimensional structure of EbfC/YbaB is highly conserved within the bacterial domain. The DNA-binding activity was observed in different bacterial species, suggesting that this protein can protect DNA during stress conditions. These findings indicate that EbfC/YbaB is a broadly distributed NAP. Here, we present a review of the existing data on this NAP.

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Nucleoid-associated proteins shape chromatin structure and transcriptional regulation across the bacterial kingdom

Cited by 51 publications

References 349 publications

Epigenetic-Mediated Antimicrobial Resistance: Host versus Pathogen Epigenetic Alterations

Epigenetic-Mediated Antimicrobial Resistance: Host versus Pathogen Epigenetic Alterations

Spatiotemporal Coupling of DNA Supercoiling and Genomic Sequence Organization—A Timing Chain for the Bacterial Growth Cycle?

EbfC/YbaB: A Widely Distributed Nucleoid-Associated Protein in Prokaryotes

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