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Phase-Variable Methylation and Epigenetic Regulation by Type I

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Phase-Variable Methylation and Epigenetic Regulation by Type I FEMS Microbiology Reviews, fux025, 41, 2017, S3–S15 doi: 10.1093/femsre/fux025 Review Article REVIEW ARTICLE Phase-variable methylation and epigenetic regulation by type I restriction–modification systems Megan De Ste Croix1,#, Irene Vacca1,#, Min Jung Kwun2,JosephD.Ralph1, Stephen D. Bentley3, Richard Haigh1, Nicholas J Croucher2 † and Marco R Oggioni1,∗, 1Department of Genetics, University of Leicester, Leicester LE1 7RH, UK, 2Department of Infectious Disease Epidemiology, Imperial College London, London W2 1PG, UK and 3Infection Genomics, Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK ∗Corresponding author: Department of Genetics, University of Leicester, University Road, Leicester LE1 7RH, UK. Tel: +44 (0)116 252 2261; E-mail [email protected] #Both authors contributed equally One sentence summary: Phase-variable type I restriction–modification systems show potential for epigenetic control of gene expression. Editor: Oscar Kuipers †Marco R Oggioni, http://orcid.org/0000-0003-4117-793X ABSTRACT Epigenetic modifications in bacteria, such as DNA methylation, have been shown to affect gene regulation, thereby generating cells that are isogenic but with distinctly different phenotypes. Restriction–modification (RM) systems contain prototypic methylases that are responsible for much of bacterial DNA methylation. This review focuses on a distinctive group of type I RM loci that , through phase variation, can modify their methylation target specificity and can thereby switch bacteria between alternative patterns of DNA methylation. Phase variation occurs at the level of the target recognition domains of the hsdS (specificity) gene via reversible recombination processes acting upon multiple hsdS alleles. We describe the global distribution of such loci throughout the prokaryotic kingdom and highlight the differences in loci structure across the various bacterial species. Although RM systems are often considered simply as an evolutionary response to bacteriophages, these multi-hsdS type I systems have also shown the capacity to change bacterial phenotypes. The ability of these RM systems to allow bacteria to reversibly switch between different physiological states, combined with the existence of such loci across many species of medical and industrial importance, highlights the potential of phase-variable DNA methylation to act as a global regulatory mechanism in bacteria. Keywords: epigenetics; restriction-modification; phase variation; DNA methylation INTRODUCTION have been characterised in addition to their initially described role as defence mechanisms against foreign DNA (Vasu and Na- It is just over 50 years since enzymatic modification and restric- garaja 2013). The main aim of this review is to summarise the tion of both bacteriophage and bacterial chromosomal DNA was information currently available about a distinct group of phase- first described (Arber and Dussoix 1962). Since then, multiple variable type I RM systems in species where there is the poten- families of DNA modification and restriction–modification (RM) tial for epigenetic effects upon bacterial gene expression and enzymes have been identified, and a wide variety of functions Received: 18 February 2017; Accepted: 9 May 2017 C FEMS 2017. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. S3 S4 FEMS Microbiology Reviews, 2017, Vol. 41, No. Supp 1 complex phenotypes (Dybvig, Sitaraman and French 1998; to Cori initiating replication of the genome, which results in the Manso et al. 2014;Liet al. 2016). General information on methy- production of hemimethylated DNA. This prevents further ex- lation systems, and phase-variable methylation systems in par- pression of dnaA, and activates a cascade of genes that are only ticular, has been reviewed in depth elsewhere (Murray 2000; expressed when GANTC is hemimethylated, which coordinate Srikhanta, Fox and Jennings 2010; Loenen et al. 2014a,b). the swarmer to stalked cell transition. One of these expressed genes is ctrA, whose protein again binds to Cori preventing DNA initiation, as well as activating the expression of CcrM and Ft- DNA METHYLATION SYSTEMS sZma (Marinus and Casadesus 2009). Once CcrM is expressed, it is able to methylate the newly synthesised DNA strands, result- DNA methylation has been shown to be an increasingly com- ing in complete methylation of the dnaA promoter again thereby mon feature of prokaryotic genomes and it is present in more allowing for a new round of DNA replication only when the one than 90% of species studied (Blow et al. 2016). Chemical mod- before has been completed (Marinus and Casadesus 2009). ification is either at an adenine or a cytosine altering the base to 6-methyladenosine (m6A), 4-methylcytosine (m4C) or 5-methylcytosine (m5C), respectively; of these modifications, RM SYSTEMS the m6A accounts for 75% all observed prokaryote methylation (Blow et al. 2016). Such DNA methylation can now be routinely Within RM systems, four families have been recognised based identified during whole-genome DNA sequencing using the sin- on their mechanism of action, recognition sequence patterns gle molecule real-time (SMRT) sequencing system developed by and enzyme structure (Loenen et al. 2014a,b). These bifunctional Pacific Biosciences (Clark et al. 2012). systems are capable of the modification of DNA bases in spe- DNA methylation modifications are generated by a methyl- cific motifs through the addition of methyl groups, as wellas transferase enzyme (MTase), which facilitates the transfer of a the degradation of DNA molecules by cleavage of the phospho- methyl group from a molecule of S-adenosyl-L-methionine onto diester backbone. The RM enzymes commonly used in the lab- the relevant base (Bheemanaik, Reddy and Rao 2006). While or- oratory are those of the type II family of enzymes (Loenen et al. phan MTases are not uncommon, MTases in bacteria are typi- 2014a) as these enzymes cleave and methylate DNA at, or close cally found within RM systems. With such RM systems, the ad- to, a fixed recognition site, typically a 4–8 bp palindromic se- dition of a methyl group to a nucleotide within a specific DNA quence (Pingoud and Jeltsch 2001; Srikhanta, Fox and Jennings target sequence then allows the DNA molecule to be recognised 2010). Type II systems are a diverse group of enzymes but usually as self, thereby protecting it from the restriction function. A ran- consist of two separate enzymes for restriction and methylation dom DNA molecule entering a cell is very unlikely to be methy- (res and mod), which recognise the same sequence. Type II en- lated in the correct pattern and therefore the cell will recog- zymes are highly heterogeneous, and include multiple enzyme nise it as foreign and, as a result, will be capable of cleaving it. families that have evolved independently. Type IIP enzymes are While the ability to recognise self-DNA is the primary purpose of the classical enzymes used in molecular biology that recognise DNA methylation for RM systems, the addition of methyl groups as self a palindromic target with methylation on both strands, to DNA can however have other effects. Indeed when a methyl while cleaving unmethylated DNA within that same target. In group is added to a base, the structure and dynamics of the DNA contrast, type IIS enzymes are less common and cleave outside molecule are altered, which may in turn result in changes in their recognition sequence (Loenen et al. 2014a). Lastly, the type DNA–protein interactions (Marinus and Casadesus 2009); such IIG enzymes are large enzymes which contain both of their en- structural changes are known to be able to regulate gene expres- zymatic activities within the same protein (Loenen et al. 2014a). sion. Similarly to the type II systems, type III RM systems are also One of the best studied of all the prokaryotic MTases is the typically encoded by mod and res genes, that are co-transcribed DNA adenine methylase (Dam) of the γ -proteobacteria (Heusipp, (Srikhanta, Fox and Jennings 2010). Methylation by a type III RM Falker¨ and Alexander Schmidt 2007; Marinus and Casadesus system is single stranded and specific; however, these RM en- 2009). This orphan MTase is responsible for the methylation zymes are less commonly used in genetic engineering as the of the four-base sequence GATC (Heusipp, Falker¨ and Alexan- cleavage site occurs 25–27 bp downstream of the 5–6 bp recogni- der Schmidt 2007; Marinus and Casadesus 2009). Methylation tion sequence (Srikhanta, Fox and Jennings 2010).TypeIRMen- of GATC in bacteria serves several functions. For example, the zymes differ from the others in that they are encoded by three addition of a methyl group to oriC promotes the binding of the separate genes, hsdR, hsdM and hsdS, determining the endonu- replication initiation complex (Wion and Casadesus´ 2006). Addi- clease, methyltransferase and specificity subunits, respectively. tionally, the hemimethylation on GATC that arises due to DNA- Type I enzymes have also fewer applications in biotechnology strand replication allows the recognition of the parent strand because though the DNA methylation occurs on both strands of from the daughter strand, meaning that replication errors can be a specific asymmetric, bi-partite sequence (Loenen et al. 2014b), identified and corrected by the cells mismatch repair machinery
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