Multiplication of a restriction–modification gene complex

Sadykov, Marat R.; Asami, Yasushi; Niki, Hironori; Handa, Nobuhiko; Itaya, Mitsuhiro; Tanokura, Masaru; Kobayashi, Ichizo

doi:10.1046/j.1365-2958.2003.03464.x

Cited by 29 publications

(45 citation statements)

References 53 publications

(80 reference statements)

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“…For example, homologous recombination can mediate competition between resident and incoming stretches of DNA Handa et al 2001;Sadykov et al 2003;Mochizuki et al 2006). Regions of DNA encoding TA-like restrictionmodification systems can displace those that do not, but not vice versa Handa et al 2001).…”

Section: Discussionmentioning

confidence: 99%

Within-host competition selects for plasmid-encoded toxin–antitoxin systems

2010

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Toxin-antitoxin (TA) systems are commonly found on bacterial plasmids. The antitoxin inhibits toxin activity unless the system is lost from the cell. Then the shorter lived antitoxin degrades and the cell becomes susceptible to the toxin. Selection for plasmid-encoded TA systems was initially thought to result from their reducing the number of plasmid-free cells arising during growth in monoculture. However, modelling and experiments have shown that this mechanism can only explain the success of plasmid TA systems under a restricted set of conditions. Previously, we have proposed and tested an alternative model explaining the success of plasmid TA systems as a consequence of competition occurring between plasmids during co-infection of bacterial hosts. Here, we test a further prediction of this model, that competition between plasmids will lead to the biased accumulation of TA systems on plasmids relative to chromosomes. Transposon-encoded TA systems were added to populations of plasmid-containing cells, such that TA systems could insert into either plasmids or chromosomes. These populations were enriched for transposon-containing cells and then incubated in environments that did, or did not, allow effective within-host plasmid competition to occur. Changes in the ratio of plasmid-to chromosome-encoded TA systems were monitored. In agreement with our model, we found that plasmid-encoded TA systems had a competitive advantage, but only when host cells were sensitive to the effect of TA systems. This result demonstrates that within-host competition between plasmids can select for TA systems.

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Section: Discussionmentioning

confidence: 99%

Within-host competition selects for plasmid-encoded toxin–antitoxin systems

2010

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“…Similarly, it was observed that an R-M gene complex residing on a bacterial chromosome cannot be replaced easily by a homologous sequence of DNA (102,103), indicating that they are difficult to eliminate. Furthermore, it was observed that R-M systems are often linked to mobile elements or acquired through HGT (99).…”

Section: Stabilization Of Genomic Islandsmentioning

confidence: 99%

Diverse Functions of Restriction-Modification Systems in Addition to Cellular Defense

Vasu

Nagaraja

2013

Microbiol Mol Biol Rev

507

481

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SUMMARY Restriction-modification (R-M) systems are ubiquitous and are often considered primitive immune systems in bacteria. Their diversity and prevalence across the prokaryotic kingdom are an indication of their success as a defense mechanism against invading genomes. However, their cellular defense function does not adequately explain the basis for their immaculate specificity in sequence recognition and nonuniform distribution, ranging from none to too many, in diverse species. The present review deals with new developments which provide insights into the roles of these enzymes in other aspects of cellular function. In this review, emphasis is placed on novel hypotheses and various findings that have not yet been dealt with in a critical review. Emerging studies indicate their role in various cellular processes other than host defense, virulence, and even controlling the rate of evolution of the organism. We also discuss how R-M systems could have successfully evolved and be involved in additional cellular portfolios, thereby increasing the relative fitness of their hosts in the population.

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“…An addiction module found on plasmids, prophages, integrons, and other mobile elements would help their stable maintenance, and, in general, an addiction module would stabilize maintenance of any linked genomic region (5,8,21,32,58,64). Indeed, a theoretical work demonstrated that an addiction module can defeat its competitor and spread in a population in the presence of space structure (47).…”

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confidence: 99%

“…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). However, the level of such killing varies among RM systems, presumably reflecting the complexity of the parasite-host interaction (and we will analyze one example in the present work).…”

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confidence: 99%

“…The selfish-gene concept is strongly supported by the finding that the multiplication of a chromosomal RM gene complex is dependent on the functional restriction gene (58). Furthermore, type II RM systems show some similarity to viruses in their requirements for regulation of gene expression (30,49,60,62,66) in that, when they enter a new host, they have to establish themselves without excessive killing of the host cells.…”

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confidence: 99%

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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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Multiplication of a restriction–modification gene complex

Cited by 29 publications

References 53 publications

Within-host competition selects for plasmid-encoded toxin–antitoxin systems

Within-host competition selects for plasmid-encoded toxin–antitoxin systems

Diverse Functions of Restriction-Modification Systems in Addition to Cellular Defense

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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