Selfish Behavior of Restriction-Modification Systems

Naito, Taku; Kusano, Kohji; Kobayashi, Ichizo

doi:10.1126/science.7846533

Cited by 342 publications

(313 citation statements)

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“…In bacteria, methylation is best studied as part of restriction-modification (R-M) systems that have long been considered as contributing to bacterial immune response against incoming DNA including phages 4 . However, recent research has suggested that R-M systems may be 'selfish' elements that protect themselves against removal, through post-segregational killing of newly born progeny by pre-existing and stable restriction enzyme molecules [5][6][7][8][9][10][11] .…”

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Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription

et al. 2012

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DnA cytosine methylation regulates gene expression in mammals. In bacteria, its role in gene expression and genome architecture is less understood. Here we perform high-throughput sequencing of bisulfite-treated genomic DnA from Escherichia coli K12 to describe, for the first time, the extent of cytosine methylation of bacterial DnA at single-base resolution. Whereas most target sites (C m CWGG) are fully methylated in stationary phase cells, many sites with an extended CC m CWGG motif are only partially methylated in exponentially growing cells. We speculate that these partially methylated sites may be selected, as these are slightly correlated with the risk of spontaneous, non-synonymous conversion of methylated cytosines to thymines. microarray analysis in a cytosine methylation-deficient mutant of E. coli shows increased expression of the stress response sigma factor Rpos and many of its targets in stationary phase. Thus, DnA cytosine methylation is a regulator of stationary phase gene expression in E. coli.

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Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription

et al. 2012

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“…Unmodified target sequences will elicit restriction and the cell will be killed. Some R-M systems therefore have been considered as 'plasmid addiction systems' (Naito et al, 1995 affect the relative stabilities of the restriction enzyme (R 2 M 2 S 1 ) and the modification component (M 2 S 1 ). If this were so, in the absence of ClpXP the loss of hsd genes, like the loss of type II R-M genes, could lead to 'programmed cell death'.…”

Section: Do Proteases Affect the Introduction Of Type I R-m Genes By mentioning

confidence: 99%

ClpX and ClpP are essential for the efficient acquisition of genes specifying type IA and IB restriction systems

Makovets

Titheradge

Murray

1998

Molecular Microbiology

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SummaryEfficient acquisition of genes that encode a restriction and modification (R-M) system with specificities different from any already present in the recipient bacterium requires the sequential production of the new modification enzyme followed by the restriction activity in order that the chromosome of the recipient bacterium is protected against attack by the restriction endonuclease. We show that ClpX and ClpP, the components of ClpXP protease, are necessary for the efficient transmission of the genes encoding EcoKI and EcoAI, representatives of two families of type I R-M systems, thus implicating ClpXP in the modulation of restriction activity. Loss of ClpX imposed a bigger barrier than loss of ClpP, consistent with a dual role for ClpX, possibly as a chaperone and as a component of the ClpXP protease. Transmission of genes specifying EcoKI was more dependent on ClpX and ClpP than transmission of the genes for EcoAI. Sensitivity to absence of the protease was also influenced by the mode of gene transfer; conjugative transfer and transformation were more dependent on ClpXP than transduction. In the absence of either ClpX or ClpP transfer of the EcoKI genes by P1-mediated transduction was impaired, transfer of the EcoAI genes was not.

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“…A third type of postsegregational killing systems consists of several type II restriction-modification (RM) systems (29,31,48). A type II RM system is typically composed of a gene encoding a DNA endonuclease (restriction enzyme), which cleaves double-stranded DNA at a specific recognition sequence, and a gene encoding a DNA methyltransferase (modification enzyme), which methylates the same recognition sequence to protect DNA from the cleavage.…”

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“…According to a hypothesis known as the cellular defense hypothesis, RM systems can provide a defense against invading foreign DNAs such as phage genomes and plasmids and may have been selected and maintained during evolution due to this benefit. Postsegregational host killing allows a plasmid carrying a type II RM gene complex to resist its elimination from host cells by a competitor genetic element (48). Such RM systems with demonstrated capacity for postsegregational killing include PaeR7I, EcoRI, EcoRV, and SsoII (7,36,48,49).…”

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confidence: 99%

“…Postsegregational host killing allows a plasmid carrying a type II RM gene complex to resist its elimination from host cells by a competitor genetic element (48). Such RM systems with demonstrated capacity for postsegregational killing include PaeR7I, EcoRI, EcoRV, and SsoII (7,36,48,49). Chromosomally placed RM gene complexes (PaeR7I and BamHI) also resist replacement by an allelic DNA (21,58).…”

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Maintenance Forced by a Restriction-Modification System Can Be Modulated by a Region in Its Modification Enzyme Not Essential for Methyltransferase Activity

et al. 2008

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Several type II restriction-modification gene complexes can force their maintenance on their host bacteria by killing cells that have lost them in a process called postsegregational killing or genetic addiction. It is likely to proceed by dilution of the modification enzyme molecule during rounds of cell division following the gene loss, which exposes unmethylated recognition sites on the newly replicated chromosomes to lethal attack by the remaining restriction enzyme molecules. This process is in apparent contrast to the process of the classical types of postsegregational killing systems, in which built-in metabolic instability of the antitoxin allows release of the toxin for lethal action after the gene loss. In the present study, we characterize a mutant form of the EcoRII gene complex that shows stronger capacity in such maintenance. This phenotype is conferred by an L80P amino acid substitution (T239C nucleotide substitution) mutation in the modification enzyme. This mutant enzyme showed decreased DNA methyltransferase activity at a higher temperature in vivo and in vitro than the nonmutated enzyme, although a deletion mutant lacking the N-terminal 83 amino acids did not lose activity at either of the temperatures tested. Under a condition of inhibited protein synthesis, the activity of the L80P mutant was completely lost at a high temperature. In parallel, the L80P mutant protein disappeared more rapidly than the wild-type protein. These results demonstrate that the capability of a restrictionmodification system in forcing maintenance on its host can be modulated by a region of its antitoxin, the modification enzyme, as in the classical postsegregational killing systems.

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Selfish Behavior of Restriction-Modification Systems

Cited by 342 publications

References 12 publications

Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription

Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription

ClpX and ClpP are essential for the efficient acquisition of genes specifying type IA and IB restriction systems

Maintenance Forced by a Restriction-Modification System Can Be Modulated by a Region in Its Modification Enzyme Not Essential for Methyltransferase Activity

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