Chromosomal position shift of a regulatory gene alters the bacterial phenotype

Gerganova, Veneta; Berger, Michael; Zaldastanishvili, Elisabed; Sobetzko, Patrick; Lafon, Corinne; Mourez, Michaël; Travers, Andrew; Muskhelishvili, Georgi

doi:10.1093/nar/gkv709

Cited by 47 publications

(56 citation statements)

References 57 publications

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“…Consistently, translocation of the fis gene to Ter‐MD sustains the overall expression level of Fis relative to wild type, but causes moderate changes in the expression levels of some genes regulated by Fis, as well as an increase in sensitivity of cells to oxidative stresses and drugs (Gerganova et al . ). Chromosomal locations of some DNA elements can, therefore, be important to strictly exert their regulatory functions.…”

Section: Discussionmentioning

confidence: 97%

Chromosomal location of the DnaA‐reactivating sequence DARS2 is important to regulate timely initiation of DNA replication in Escherichia coli

et al. 2016

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In Escherichia coli, the initiator protein ATP-DnaA promotes initiation of chromosome replication in a timely manner. After initiation, DnaA-bound ATP is hydrolyzed to yield ADP-DnaA, which is inactive in initiation. DnaA-reactivating sequences (DARS1 and DARS2) on the chromosome have predominant roles in catalysis of nucleotide exchange, producing ATP-DnaA from ADP-DnaA, which is prerequisite for timely initiation. Both DARS sequences have a core region containing a cluster of three DnaA-binding sites. DARS2 is more effective in vivo than DARS1, and timely activation of DARS2 depends on binding of two nucleoid-associated proteins, IHF and Fis. DARS2 is located centrally between the chromosomal replication origin oriC and the terminus region terC. We constructed mutants in which DARS2 was translocated to several chromosomal loci, including sites proximal to oriC and to terC. Replication initiation was inhibited in cells in which DARS2 was translocated to terCproximal sites when the cells were grown at 42°C, although overall binding efficiency of IHF and Fis to the translocated DARS2 was not affected. Inhibition was largely sustained even in cells lacking MatP, a DNA-binding protein responsible for terC-specific subchromosomal structure. These results suggest that functional regulation of DARS2 is correlated with its chromosomal location under certain conditions.

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Section: Discussionmentioning

confidence: 97%

Chromosomal location of the DnaA‐reactivating sequence DARS2 is important to regulate timely initiation of DNA replication in Escherichia coli

et al. 2016

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“…Another DNA binding protein, the leucine-responsive regulatory protein, Lrp, contributes by stimulating transcription of P ilvIH (Wang et al 1993) A gene may not have to leave its original host cell to experience new patterns of DNA topological influence. Simply repositioning the gene on the single, circular chromosome of the bacterium may achieve this effect (Brambilla and Sclavi 2015;Fitzgerald et al 2015;Gerganova et al 2015). Bioinformatic analyses and experimental work have indicated that gene location can affect expression for reasons other than gene dosage (i.e.…”

Section: Dna Supercoiling Bacterial Evolution and Pathogenesismentioning

confidence: 99%

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Dorman

2016

Biophys Rev

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Although it has become routine to consider DNA in terms of its role as a carrier of genetic information, it is also an important contributor to the control of gene expression. This regulatory principle arises from its structural properties. DNA is maintained in an underwound state in most bacterial cells and this has important implications both for DNA storage in the nucleoid and for the expression of genetic information. Underwinding of the DNA through reduction in its linking number potentially imparts energy to the duplex that is available to drive DNA transactions, such as transcription, replication and recombination. The topological state of DNA also influences its affinity for some DNA binding proteins, especially in DNA sequences that have a high A + T base content. The underwinding of DNA by the ATP-dependent topoisomerase DNA gyrase creates a continuum between metabolic flux, DNA topology and gene expression that underpins the global response of the genome to changes in the intracellular and external environments. These connections describe a fundamental and generalised mechanism affecting global gene expression that underlies the specific control of transcription operating through conventional transcription factors. This mechanism also provides a basal level of control for genes acquired by horizontal DNA transfer, assisting microbial evolution, including the evolution of pathogenic bacteria.

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“…Furthermore, the ribosomal RNAs showing this methylation pattern were localized near the origin of replication. Genomic position does effect expression levels (Gerganova et al , 2015; Muskhelishvili & Travers, 2013).…”

Section: Discussionmentioning

confidence: 99%

Comparison ofYersinia enterocoliticaDNA methylation at ambient and host temperatures

Hofwegen

Hovde

Minnich

2019

Preprint

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10Pathogenic bacteria recognize environmental cues to vary gene expression for host adaptation. 11Moving from ambient to host temperature, Yersinia enterocolitica responds by immediately 12repressing flagella synthesis and inducing the virulence plasmid (pYV)-encoded type III secretion 13 system. In contrast, shifting from host to ambient temperature requires 2.5 generations to restore 14 motility suggesting a link to the cell cycle. We hypothesized that differential DNA methylation 15 contributes to temperature-regulated gene expression. We tested this hypothesis by comparing 16 single-molecule real-time (SMRT) sequencing of Y. enterocolitica DNA from cells growing 17 exponentially at 22°C and 37°C. The inter-pulse duration ratio rather than the traditional QV scoring 18 was the kinetic metric to compare DNA from cells grown at each temperature. All 565 YenI 19 restriction sites were fully methylated at both temperatures. Among the 27,118 DNA adenine 20 methylase (Dam) sites, 42 had differential methylation patterns while 17 remained unmethylated 21 regardless of temperature. A subset of the differentially methylated Dam sites localized to promoter 22 regions of predicted regulatory genes including LysR-type and PadR-like transcriptional regulators, 23 and a cyclic-di-GMP phosphodiesterase. The unmethylated Dam sites localized with a bias to the 24 replication terminus, suggesting they were protected from Dam methylase. No cytosine methylation 25 was detected at Dcm sites. 26 27 28 DATA SUMMARY 29 30 All methylation/base modification data are available at figshare at 31 https://dx.doi.org/10.6084/m9.figshare.3493247 and 32 https://dx.doi.org/10.6084/m9.figshare.3493310. 33 34 35 IMPACT STATEMENT 36 37 Organisms sense and respond to their environment, in part, by epigenetic variation mediated by 38 DNA methylation. Pathogenic bacteria vary gene expression to allow survival and activate virulence 39 systems in response to host temperature. Yersinia enterocolitica, a facultative intracellular 40 pathogen, respond by immediately repressing flagella synthesis and inducing the virulence plasmid-41 encoded type III secretion system. In this work, we examined the locations of DNA methylation 42 throughout the Y. enterocolitica genome. While most methylation target sites were fully methylated, 43 we identified sites with disparate temperature-dependent methylation. Several of these sites were 44 within promoter regions of predicted regulatory genes. Differences in DNA methylation in promoter 45 sequences are often responsible for variations in transcription. Identification of these differences in 46 methylation provide likely candidates for regulators responsible for temperature-dependent 47 phenotypes. 48 49 50

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Chromosomal position shift of a regulatory gene alters the bacterial phenotype

Cited by 47 publications

References 57 publications

Chromosomal location of the DnaA‐reactivating sequence DARS2 is important to regulate timely initiation of DNA replication in Escherichia coli

Chromosomal location of the DnaA‐reactivating sequence DARS2 is important to regulate timely initiation of DNA replication in Escherichia coli

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Comparison ofYersinia enterocoliticaDNA methylation at ambient and host temperatures

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