The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection

Zaleski, Piotr; Wojciechowski, Marek; Piekarowicz, Andrzej

doi:10.1099/mic.0.28184-0

Cited by 81 publications

(76 citation statements)

References 34 publications

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“…Phase variation is a mechanism that has been shown to provide transient resistance to phage infection for Gram-negative bacteria (14,65). We identified seven unique putative phase variant mutations in this study, two of which were each found in two separate mutant strains.…”

Section: Discussionmentioning

confidence: 93%

Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption

Denes

Bakker

Tokman

et al. 2015

Appl Environ Microbiol

104

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Listeria-infecting phages are readily isolated from Listeria-containing environments, yet little is known about the selective forces they exert on their host. Here, we identified that two virulent phages, LP-048 and LP-125, adsorb to the surface of Listeria monocytogenes strain 10403S through different mechanisms. We isolated and sequenced, using whole-genome sequencing, 69 spontaneous mutant strains of 10403S that were resistant to either one or both phages. Mutations from 56 phage-resistant mutant strains with only a single mutation mapped to 10 genes representing five loci on the 10403S chromosome. An additional 12 mutant strains showed two mutations, and one mutant strain showed three mutations. Two of the loci, containing seven of the genes, accumulated the majority (n ‫؍‬ 64) of the mutations. A representative mutant strain for each of the 10 genes was shown to resist phage infection through mechanisms of adsorption inhibition. Complementation of mutant strains with the associated wild-type allele was able to rescue phage susceptibility for 6 out of the 10 representative mutant strains. Wheat germ agglutinin, which specifically binds to N-acetylglucosamine, bound to 10403S and mutant strains resistant to LP-048 but did not bind to mutant strains resistant to only LP-125. We conclude that mutant strains resistant to only LP-125 lack terminal N-acetylglucosamine in their wall teichoic acid (WTA), whereas mutant strains resistant to both phages have disruptive mutations in their rhamnose biosynthesis operon but still possess N-acetylglucosamine in their WTA. V irulent phages have been shown to present a tremendous selective pressure on their bacterial host populations. Not only is phage predation a major driver of bacterial diversification (1, 2), but it may also select for hypermutators, which could increase the frequency of mutations in bacterial populations (3, 4). Whereas bacteria are limited to one cell division per generation, a single phage-infected cell can produce a burst ranging from less than 5 to over 1,000 progeny phages in a similar period of time (5-7). Phages consequently have the capability to rapidly outgrow their bacterial hosts and can significantly reduce or eliminate susceptible bacteria in the local environment (8, 9). Therefore, the potential for bacterial strains to persist in an environment containing lytic phages may be contingent upon that strain accumulating spontaneous mutations that grant resistance to phage infection (10). These phage-resistant mutant strains most typically resist phage infection through mechanisms of adsorption inhibition, i.e., alterations of the cell surface that affect phage attachment (11). However, one study reported that nearly all phage-resistant mutant strains of Streptococcus thermophilus had acquired CRISPR spacers that matched invading phage genomes (12); these S. thermophilus mutant strains would be expected to resist phage infection after the adsorption step. Phage-resistant mutant strains that resist infection through mechanisms of adsorption inh...

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Section: Discussionmentioning

confidence: 93%

Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption

Denes

Bakker

Tokman

et al. 2015

Appl Environ Microbiol

104

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“…Bacteria can switch on or off the expression of phage receptors 105,106 or secrete polysaccharides that limit the access to the receptor 107 . Bacterial hosts can also express membrane proteins that prevent injection of the viral genetic material into the cell 108 .…”

Section: Mechanisms Of Antiviral Defence In Prokaryotesmentioning

confidence: 99%

CRISPR-Cas immunity in prokaryotes

Marraffini

2015

Nature

699

486

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Prokaryotic organisms are threatened by a large array of viruses and have developed numerous defence strategies. Among these, only clustered, regularly interspaced short palindromic repeat (CRISPR)-Cas systems provide adaptive immunity against foreign elements. Upon viral injection, a small sequence of the viral genome, known as a spacer, is integrated into the CRISPR locus to immunize the host cell. Spacers are transcribed into small RNA guides that direct the cleavage of the viral DNA by Cas nucleases. Immunization through spacer acquisition enables a unique form of evolution whereby a population not only rapidly acquires resistance to its predators but also passes this resistance mechanism vertically to its progeny.

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“…The effectiveness of RM systems in host protection against phage infection has been demonstrated in various studies reporting 10-to 10 8 -fold protection against phage infection (reviewed in reference 34). Interestingly, the expression of many RM systems is phase variable (35)(36)(37)(38), which has important evolutionary implications, which are discussed below.…”

Section: Restriction-modificationmentioning

confidence: 99%

Evolutionary Ecology of Prokaryotic Immune Mechanisms

Houte

Buckling

Westra

2016

Microbiol Mol Biol Rev

223

177

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SUMMARYBacteria have a range of distinct immune strategies that provide protection against bacteriophage (phage) infections. While much has been learned about the mechanism of action of these defense strategies, it is less clear why such diversity in defense strategies has evolved. In this review, we discuss the short- and long-term costs and benefits of the different resistance strategies and, hence, the ecological conditions that are likely to favor the different strategies alone and in combination. Finally, we discuss some of the broader consequences, beyond resistance to phage and other genetic elements, resulting from the operation of different immune strategies.

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The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection

Cited by 81 publications

References 34 publications

Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption

Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption

CRISPR-Cas immunity in prokaryotes

Evolutionary Ecology of Prokaryotic Immune Mechanisms

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