Avoidance of recognition sites of restriction-modification systems is a widespread but not universal anti-restriction strategy of prokaryotic viruses

Rusinov, Ivan S.; Ershova, Anna S.; Karyagina, A. S.; Spirin, Sergei A.; Alexeevski, Andrei V.

doi:10.1186/s12864-018-5324-3

Cited by 39 publications

(49 citation statements)

References 37 publications

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“…Type I R-M is a ubiquitous defensive system to combat invasive foreign DNA. Bacteriophages have evolved numerous mechanisms to circumvent restriction by R-M systems, including encoding anti-restriction proteins in their genomes and limiting the number of recognition sites ( 15 ). Bacteria in turn continue to evolve systems to counteract phage escape.…”

Section: Introductionmentioning

confidence: 99%

Analysis of a phase-variable restriction modification system of the human gut symbiont Bacteroides fragilis

Ben-Assa

Coyne

Fomenkov

et al. 2020

Nucleic Acids Research

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The genomes of gut Bacteroidales contain numerous invertible regions, many of which contain promoters that dictate phase-variable synthesis of surface molecules such as polysaccharides, fimbriae, and outer surface proteins. Here, we characterize a different type of phase-variable system of Bacteroides fragilis, a Type I restriction modification system (R-M). We show that reversible DNA inversions within this R-M locus leads to the generation of eight specificity proteins with distinct recognition sites. In vitro grown bacteria have a different proportion of specificity gene combinations at the expression locus than bacteria isolated from the mammalian gut. By creating mutants, each able to produce only one specificity protein from this region, we identified the R-M recognition sites of four of these S-proteins using SMRT sequencing. Transcriptome analysis revealed that the locked specificity mutants, whether grown in vitro or isolated from the mammalian gut, have distinct transcriptional profiles, likely creating different phenotypes, one of which was confirmed. Genomic analyses of diverse strains of Bacteroidetes from both host-associated and environmental sources reveal the ubiquity of phase-variable R-M systems in this phylum.

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Section: Introductionmentioning

confidence: 99%

Analysis of a phase-variable restriction modification system of the human gut symbiont Bacteroides fragilis

Ben-Assa

Coyne

Fomenkov

et al. 2020

Nucleic Acids Research

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“…Recognition sites of type II R-M systems are nearly always an inverted repeat (Rusinov et al 2015;Gelfand and Koonin 1997), and therefore one recognition site induces one single taboo. This is specially interesting because, according to Rusinov et al (2015Rusinov et al ( , 2018a, only type II R-M systems induce taboos.…”

Section: Examples Of Plausible Bacterial Taboo-setsmentioning

confidence: 99%

“…Among the 3623 bacteria in REBASE (2020a), only 465 have more than three type II restriction enzymes. Assuming that only type II restriction enzymes induce taboos, as stated by Rusinov et al (2015Rusinov et al ( , 2018a, Corollary 25.b implies that at least 87% (3158/3623) of bacterial taboo-sets in REBASE (2020a) yield connected taboo-free Hamming graphs. Similarly, at least 90% (139/153) of archea in REBASE (2020b) induce connected taboo-free Hamming graphs, because they have less than four type II restriction enzymes.…”

Section: A Frequent Case: Turneriella Parvamentioning

confidence: 99%

“…Nevertheless, Gelfand and Koonin (1997) and Rocha et al (2001) found a significant avoidance of recognition sites in bacterial DNA, and Rusinov et al (2015) showed that this avoidance was characteristic of type II R-M systems. Also in bacteriophages, the avoidance of the recognition sites is evolutionary advantageous (Rocha et al 2001), mainly for non-temperate bacteriophages affected by orthodox type II R-M systems (Rusinov et al 2018a). Therefore in those instances the recognition site is, as we call it, a taboo for host and foreign DNA.…”

Section: Introductionmentioning

confidence: 99%

“… 2001 ), mainly for non-temperate bacteriophages affected by orthodox type II R–M systems (Rusinov et al. 2018a ). Therefore in those instances the recognition site is, as we call it, a taboo for host and foreign DNA.…”

Section: Introductionmentioning

confidence: 99%

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Structure of the space of taboo-free sequences

Manuel

Haeseler

2020

J. Math. Biol.

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Models of sequence evolution typically assume that all sequences are possible. However, restriction enzymes that cut DNA at specific recognition sites provide an example where carrying a recognition site can be lethal. Motivated by this observation, we studied the set of strings over a finite alphabet with taboos, that is, with prohibited substrings. The taboo-set is referred to as $$\mathbb {T}$$ T and any allowed string as a taboo-free string. We consider the so-called Hamming graph $$\varGamma _n(\mathbb {T})$$ Γ n ( T ) , whose vertices are taboo-free strings of length n and whose edges connect two taboo-free strings if their Hamming distance equals one. Any (random) walk on this graph describes the evolution of a DNA sequence that avoids taboos. We describe the construction of the vertex set of $$\varGamma _n(\mathbb {T})$$ Γ n ( T ) . Then we state conditions under which $$\varGamma _n(\mathbb {T})$$ Γ n ( T ) and its suffix subgraphs are connected. Moreover, we provide an algorithm that determines if all these graphs are connected for an arbitrary $$\mathbb {T}$$ T . As an application of the algorithm, we show that about $$87\%$$ 87 % of bacteria listed in REBASE have a taboo-set that induces connected taboo-free Hamming graphs, because they have less than four type II restriction enzymes. On the other hand, four properly chosen taboos are enough to disconnect one suffix subgraph, and consequently connectivity of taboo-free Hamming graphs could change depending on the composition of restriction sites.

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Overcoming Bacteriophage Contamination in Bioprocessing: Strategies and Applications

Zou,

Mo,

Wang

et al. 2024

Small Methods

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Bacteriophage contamination has a devastating impact on the viability of bacterial hosts and can significantly reduce the productivity of bioprocesses in biotechnological industries. The consequences range from widespread fermentation failure to substantial economic losses, highlighting the urgent need for effective countermeasures. Conventional prevention methods, which focus primarily on the physical removal of bacteriophages from equipment, bioprocess units, and the environment, have proven ineffective in preventing phage entry and contamination. The coevolutionary dynamics between phages and their bacterial hosts have spurred the development of a diverse repertoire of antiviral defense mechanisms within microbial communities. These naturally occurring defense strategies can be harnessed through genetic engineering to convert phage‐sensitive hosts into robust, phage‐resistant cell factories, providing a strategic approach to mitigate the threats posed by bacteriophages to industrial bacterial processes. In this review, an overview of the various defense strategies and immune systems that curb the propagation of bacteriophages and highlight their applications in fermentation bioprocesses to combat phage contamination is provided. Additionally, the tactics employed by phages to circumvent these defense strategies are also discussed, as preventing the emergence of phage escape mutants is a key component of effective contamination management.

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Avoidance of recognition sites of restriction-modification systems is a widespread but not universal anti-restriction strategy of prokaryotic viruses

Cited by 39 publications

References 37 publications

Analysis of a phase-variable restriction modification system of the human gut symbiont Bacteroides fragilis

Analysis of a phase-variable restriction modification system of the human gut symbiont Bacteroides fragilis

Structure of the space of taboo-free sequences

Overcoming Bacteriophage Contamination in Bioprocessing: Strategies and Applications

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