DNA methylation by three Type I restriction modification systems of <i>Escherichia coli</i> does not influence gene regulation of the host bacterium

Mehershahi, Kurosh S.; Chen, Swaine L.

doi:10.1093/nar/gkab530

Cited by 6 publications

(6 citation statements)

References 106 publications

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“…Attempts to confirm the involvement of global genome methylation in gene regulation by creating methylation‐deficient mutants have been reported in other studies, yet the results were contradictory. Xu et al ( 2021 ) reported that uropathogenic E. coli lacking adenine methylation exhibited significant defects in persister formation during exposure to various antibiotics and stresses, whereas another study by Mehershahi and Chen ( 2021 ) reported that knocking out a type I RM system in an E. coli strain did not affect gene regulation and the performance of the mutant. Their findings suggest that not all RM systems and global methylation patterns function in a regulatory capacity.…”

Section: Discussionmentioning

confidence: 99%

Interplay of intracellular and trans‐cellular DNA methylation in natural archaeal consortia

Reva,

La Cono,

Crisafi

et al. 2024

Environ Microbiol Rep

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DNA methylation serves a variety of functions across all life domains. In this study, we investigated archaeal methylomics within a tripartite xylanolytic halophilic consortium. This consortium includes Haloferax lucertense SVX82, Halorhabdus sp. SVX81, and an ectosymbiotic Candidatus Nanohalococcus occultus SVXNc, a nano‐sized archaeon from the DPANN superphylum. We utilized PacBio SMRT and Illumina cDNA sequencing to analyse samples from consortia of different compositions for methylomics and transcriptomics. Endogenous cTAG methylation, typical of Haloferax, was accompanied in this strain by methylation at four other motifs, including GDGcHC methylation, which is specific to the ectosymbiont. Our analysis of the distribution of methylated and unmethylated motifs suggests that autochthonous cTAG methylation may influence gene regulation. The frequency of GRAGAaG methylation increased in highly expressed genes, while CcTTG and GTCGaGG methylation could be linked to restriction‐modification (RM) activity. Generally, the RM activity might have been reduced during the evolution of this archaeon to balance the protection of cells from intruders, the reduction of DNA damage due to self‐restriction in stressful environments, and the benefits of DNA exchange under extreme conditions. Our methylomics, transcriptomics and complementary electron cryotomography (cryo‐ET) data suggest that the nanohaloarchaeon exports its methyltransferase to methylate the Haloferax genome, unveiling a new aspect of the interaction between the symbiont and its host.

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Section: Discussionmentioning

confidence: 99%

Interplay of intracellular and trans‐cellular DNA methylation in natural archaeal consortia

Reva,

La Cono,

Crisafi

et al. 2024

Environ Microbiol Rep

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“…Recently, the effect of inactivation of archetypal Type I RM encoded by E. coli on gene expression was investigated. Authors demonstrated that the inactivation of three Type I MTases in different E. coli strains had no impact on gene regulation or on cellular phenotype among >1,000 growth conditions tested ( Mehershahi and Chen, 2021 ). The data suggest that the canonical Type I RM systems are involved in host defense mechanisms, without secondary regulatory functions in host physiology and virulence.…”

Section: Discussionmentioning

confidence: 99%

Phase-variable Type I methyltransferase M.NgoAV from Neisseria gonorrhoeae FA1090 regulates phasevarion expression and gonococcal phenotype

Adamczyk-Popławska

Bącal²,

Mrozek³

et al. 2022

Front. Microbiol.

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The restriction-modification (RM) systems are compared to a primitive, innate, prokaryotic immune system, controlling the invasion by foreign DNA, composed of methyltransferase (MTase) and restriction endonuclease. The biological significance of RM systems extends beyond their defensive function, but the data on the regulatory role of Type I MTases are limited. We have previously characterized molecularly a non-canonical Type I RM system, NgoAV, with phase-variable specificity, encoded by Neisseria gonorrhoeae FA1090. In the current work, we have investigated the impact of methyltransferase NgoAV (M.NgoAV) activity on gonococcal phenotype and on epigenetic control of gene expression. For this purpose, we have constructed and studied genetic variants (concerning activity and specificity) within M.NgoAV locus. Deletion of M.NgoAV or switch of its specificity had an impact on phenotype of N. gonorrhoeae. Biofilm formation and planktonic growth, the resistance to antibiotics, which target bacterial peptidoglycan or other antimicrobials, and invasion of human epithelial host cells were affected. The expression of genes was deregulated in gonococcal cells with knockout M.NgoAV gene and the variant with new specificity. For the first time, the existence of a phasevarion (phase-variable regulon), directed by phase-variable Type I MTase, is demonstrated.

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“…This enzyme plays roles in various cellular processes, including DNA repair, the regulation of gene expression, and protection against foreign DNA [10]. In certain strains of E. coli, the DNA methyltransferase EcoKI, a type I restriction-modification enzyme that methylates the adenine residues in the specific DNA sequences AAC(N6)GTGC and GCAC(N6)GTT, has been well described for its importance in protecting the bacterial DNA from being cleaved by the restriction enzyme EcoKI (HsdR), which recognizes the same DNA sequence but cuts unmethylated DNA [11]. In Alphaproteobacteria, most of the actual knowledge on DNA MTases is focused on CcrM, a type IV MTase which methylates the adenine residue of the motif GANTC [12,13].…”

Section: Dna Methylation Pattern Is Involved In Core Cellular Processesmentioning

confidence: 99%

Moving toward the Inclusion of Epigenomics in Bacterial Genome Evolution: Perspectives and Challenges

Passeri,

Vaccaro,

Mengoni

et al. 2024

IJMS

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The universality of DNA methylation as an epigenetic regulatory mechanism belongs to all biological kingdoms. However, while eukaryotic systems have been the primary focus of DNA methylation studies, the molecular mechanisms in prokaryotes are less known. Nevertheless, DNA methylation in prokaryotes plays a pivotal role in many cellular processes such as defense systems against exogenous DNA, cell cycle dynamics, and gene expression, including virulence. Thanks to single-molecule DNA sequencing technologies, genome-wide identification of methylated DNA is becoming feasible on a large scale, providing the possibility to investigate more deeply the presence, variability, and roles of DNA methylation. Here, we present an overview of the multifaceted roles of DNA methylation in prokaryotes and suggest research directions and tools which can enable us to better understand the contribution of DNA methylation to prokaryotic genome evolution and adaptation. In particular, we emphasize the need to understand the presence and role of transgenerational inheritance, as well as the impact of epigenomic signatures on adaptation and genome evolution. Research directions and the importance of novel computational tools are underlined.

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DNA methylation by three Type I restriction modification systems of Escherichia coli does not influence gene regulation of the host bacterium

Cited by 6 publications

References 106 publications

Interplay of intracellular and trans‐cellular DNA methylation in natural archaeal consortia

Interplay of intracellular and trans‐cellular DNA methylation in natural archaeal consortia

Phase-variable Type I methyltransferase M.NgoAV from Neisseria gonorrhoeae FA1090 regulates phasevarion expression and gonococcal phenotype

Moving toward the Inclusion of Epigenomics in Bacterial Genome Evolution: Perspectives and Challenges

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