Phase variation controls expression of <i>Salmonella</i> lipopolysaccharide modification genes by a DNA methylation‐dependent mechanism

Broadbent, Sarah E.; Davies, Mark R.; Woude, Marjan W. van der

doi:10.1111/j.1365-2958.2010.07203.x

Cited by 123 publications

(154 citation statements)

References 61 publications

(123 reference statements)

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“…The epigenetic regulation of PV has been best described for the Dam methyltransferase found in diverse bacteria such as E. coli and Salmonella spp. (9,46). Three systems for epigenetic PV with the participation of Dam are now known, and all require ad- 3 H]AdoMet, were digested with BstUI, and the resulting fragments were separated by electrophoresis on an 18% polyacrylamide gel.…”

Section: Discussionmentioning

confidence: 99%

Deletion of One Nucleotide within the Homonucleotide Tract Present in the hsdS Gene Alters the DNA Sequence Specificity of Type I Restriction-Modification System NgoAV

2011

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As a result of a frameshift mutation, the hsdS locus of the NgoAV type IC restriction and modification (RM) system comprises two genes, hsdS NgoAV1 and hsdS NgoAV2 . The specificity subunit, HsdS NgoAV , the product of the hsdS NgoAV1 gene, is a naturally truncated form of an archetypal specificity subunit (208 N-terminal amino acids instead of 410). The presence of a homonucleotide tract of seven guanines (poly[G]) at the 3 end of the hsdS NgoAV1 gene makes the NgoAV system a strong candidate for phase variation, i.e., stochastic addition or reduction in the guanine number. We have constructed mutants with 6 guanines instead of 7 and demonstrated that the deletion of a single nucleotide within the 3 end of the hsdS NgoAV1 gene restored the fusion between the hsdS NgoAV1 and hsdS NgoAV2 genes. We have demonstrated that such a contraction of the homonucleotide tract may occur in vivo: in a Neisseria gonorrhoeae population, a minor subpopulation of cells appeared to have only 6 guanines at the 3 end of the hsdS NgoAV1 gene. Escherichia coli cells carrying the fused gene and expressing the NgoAV⌬ RM system were able to restrict phage at a level comparable to that for the wild-type NgoAV system. NgoAV recognizes the quasipalindromic interrupted sequence 5-GCA(N 8 )TGC-3 and methylates both strands. NgoAV⌬ recognizes DNA sequences 5-GCA(N 7 )GTCA-3 and 5-GCA(N 7 )CTCA-3, although the latter sequence is methylated only on the complementary strand within the 5-CTCA-3 region of the second recognition target sequence.Restriction and modification (RM) systems are composed of two enzymatic activities that recognize the same specific DNA sequence. The restriction endonuclease cleaves the DNA, unless the recognized sequence is methylated by the modification methylase. RM systems are found in a wide variety of bacteria and archaea, and their main role is to protect cells from bacteriophage infections or the uptake of undesirable foreign DNA (7, 33). The importance of RM systems in host protection is difficult to estimate in the case of bacteria for which no phages or no phage detection methods are known and that encode several RM systems, such as Neisseria gonorrhoeae (43,34). Recently, a new role for RM systems as factors regulating other gene expression was proposed for type III RM systems (16,42).Type I DNA RM systems are multimeric enzyme complexes that recognize and methylate an adenine residue within a specific DNA sequence. The cleavage of double-stranded DNA takes place at an undefined region, several hundreds to thousands of base pairs away from the recognized sequence. The archetypal type I methyltransferases are encoded by two genes, hsdS and hsdM, and are composed of one HsdS subunit and two HsdM subunits. The HsdS subunit is responsible for recognition and binding of DNA by the enzymatic complex and for the interaction of the other subunits of the enzyme. The

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Section: Discussionmentioning

confidence: 99%

Deletion of One Nucleotide within the Homonucleotide Tract Present in the hsdS Gene Alters the DNA Sequence Specificity of Type I Restriction-Modification System NgoAV

2011

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“…OxyR induces the expression of virulence factors that allow pathogens to evade host innate immunity (74,90), while PerR has been shown to directly regulate an extracellular virulence factor (mitogen factor 3) in Streptococcus pyogenes (117). Other clinically relevant processes, such as biofilm formation (99,119) and the oxidation state-independent regulation of several epigenetically controlled promoters determining phase variation (9,113,114), are also regulated by OxyR.…”

Section: Role Of Oxyr Perr and Ohrr In Virulencementioning

confidence: 99%

Peroxide-Sensing Transcriptional Regulators in Bacteria

2012

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The ability to maintain intracellular concentrations of toxic reactive oxygen species (ROS) within safe limits is essential for all aerobic life forms. In bacteria, as well as other organisms, ROS are produced during the normal course of aerobic metabolism, necessitating the constitutive expression of ROS scavenging systems. However, bacteria can also experience transient high-level exposure to ROS derived either from external sources, such as the host defense response, or as a secondary effect of other seemingly unrelated environmental stresses. Consequently, transcriptional regulators have evolved to sense the levels of ROS and coordinate the appropriate oxidative stress response. Three well-studied examples of these are the peroxide responsive regulators OxyR, PerR, and OhrR. OxyR and PerR are sensors of primarily H 2 O 2 , while OhrR senses organic peroxide (ROOH) and sodium hypochlorite (NaOCl). OxyR and OhrR sense oxidants by means of the reversible oxidation of specific cysteine residues. In contrast, PerR senses H 2 O 2 via the Fe-catalyzed oxidation of histidine residues. These transcription regulators also influence complex biological phenomena, such as biofilm formation, the evasion of host immune responses, and antibiotic resistance via the direct regulation of specific proteins.

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“…Dam-dependent phase variation in E. coli also accounts for changes in another antigen, Ag43 (130). A third example of a surface component regulated in this way involves Salmonella lipopolysaccharide modification genes (35). Hence, a population of bacteria can consist of subpopulations whose methylation pattern and gene expression are determined by epigenetic processes.…”

Section: Genetic Heterogeneity Within Populationsmentioning

confidence: 99%

Culture History and Population Heterogeneity as Determinants of Bacterial Adaptation: the Adaptomics of a Single Environmental Transition

Ryall

Eydallin

Ferenci

2012

Microbiol Mol Biol Rev

140

109

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SUMMARY Diversity in adaptive responses is common within species and populations, especially when the heterogeneity of the frequently large populations found in environments is considered. By focusing on events in a single clonal population undergoing a single transition, we discuss how environmental cues and changes in growth rate initiate a multiplicity of adaptive pathways. Adaptation is a comprehensive process, and stochastic, regulatory, epigenetic, and mutational changes can contribute to fitness and overlap in timing and frequency. We identify culture history as a major determinant of both regulatory adaptations and microevolutionary change. Population history before a transition determines heterogeneities due to errors in translation, stochastic differences in regulation, the presence of aged, damaged, cheating, or dormant cells, and variations in intracellular metabolite or regulator concentrations. It matters whether bacteria come from dense, slow-growing, stressed, or structured states. Genotypic adaptations are history dependent due to variations in mutation supply, contingency gene changes, phase variation, lateral gene transfer, and genome amplifications. Phenotypic adaptations underpin genotypic changes in situations such as stress-induced mutagenesis or prophage induction or in biofilms to give a continuum of adaptive possibilities. Evolutionary selection additionally provides diverse adaptive outcomes in a single transition and generally does not result in single fitter types. The totality of heterogeneities in an adapting population increases the chance that at least some individuals meet immediate or future challenges. However, heterogeneity complicates the adaptomics of single transitions, and we propose that subpopulations will need to be integrated into future population biology and systems biology predictions of bacterial behavior.

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Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation‐dependent mechanism

Cited by 123 publications

References 61 publications

Deletion of One Nucleotide within the Homonucleotide Tract Present in the hsdS Gene Alters the DNA Sequence Specificity of Type I Restriction-Modification System NgoAV

Deletion of One Nucleotide within the Homonucleotide Tract Present in the hsdS Gene Alters the DNA Sequence Specificity of Type I Restriction-Modification System NgoAV

Peroxide-Sensing Transcriptional Regulators in Bacteria

Culture History and Population Heterogeneity as Determinants of Bacterial Adaptation: the Adaptomics of a Single Environmental Transition

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