Phase variation of a Type IIG restriction-modification enzyme alters site-specific methylation patterns and gene expression in Campylobacter jejuni strain NCTC11168

Nucleic Acids Research

Volumn 44, Issue 10, 2016, Pages 4581-4594

  Anjum, Awais ^a   Brathwaite, Kelly J ^b   Aidley, Jack ^a   Connerton, Phillippa L ^b   Cummings, Nicola J ^b   Parkhill, Julian ^c   Connerton, Ian ^b   Bayliss, Christopher D ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RESTRICTION ENDONUCLEASE; TYPE IIG RESTRICTION MODIFICATION ENZYME; UNCLASSIFIED DRUG; ADENINE; BACTERIAL PROTEIN; SITE SPECIFIC DNA METHYLTRANSFERASE (ADENINE SPECIFIC);

ALLELE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CAMPYLOBACTER JEJUNI; CHEMICAL PHENOMENA; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; GENE EXPRESSION; GENETIC TRANSCRIPTION; MUTANT; NONHUMAN; PHASE VARIATION; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RNA SEQUENCE; BACTERIOPHAGE; BACTERIUM ADHERENCE; BIOFILM; CACO-2 CELL LINE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYLOGENY;

ADENINE; BACTERIAL ADHESION; BACTERIAL PROTEINS; BACTERIOPHAGES; BIOFILMS; CACO-2 CELLS; CAMPYLOBACTER JEJUNI; DNA METHYLATION; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MUTATION; PHYLOGENY; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC);

EID: 84971275767     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw019     Document Type: Article

References (53)

1. Ruiz-Palacios, G. M. (2007) The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clin. Infect. Dis., 44, 701-703.
2. Tam, C. C., O'Brien, S. J., Tompkins, D. S., Bolton, F. J., Berry, L., Dodds, J., Choudhury, D., Halstead, F., Iturriza-G ómara, M., Mather, K. et al. (2012) Changes in causes of acute gastroenteritis in the United Kingdom over 15 years: Microbiologic findings from 2 prospective, population-based studies of infectious intestinal disease. Clin. Infect. Dis., 54, 1275-1286.
3. Sheppard, S. K., Dallas, J. F., Strachan, N. J. C., MacRae, M., McCarthy, N. D., Wilson, D. J., Gormley, F. J. (2009) Campylobacter genotyping to determine the source of human infection. Clin. Infect. Dis., 48, 1072-1078.
4. Hermans, D., Pasmans, F., Messens, W., Martel, A., Van Immerseel, F., Rasschaert, G., Heyndrickx, M., Van Deun, K., Haesebrouck, F. (2012) Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector Borne Zoonotic Dis., 12, 89-98.
5. Newell, D. G., Elvers, K. T., Dopfer, D., Hansson, I., Jones, P., James, S., Gittins, J., Stern, N. J., Davies, R., Connerton, I. et al. (2011) Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl. Environ. Microbiol., 77, 8605-8614.
6. Bayliss, C. D. (2009) Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals. FEMS Microbiol. Rev., 33, 504-520.
7. Parkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T., Holroyd, S. et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature, 403, 665-668.
8. Bayliss, C. D., Bidmos, F. A., Anjum, A., Manchev, V. T., Richards, R. L., Grossier, J. P., Wooldridge, K. G., Ketley, J. M., Barrow, P. A., Jones, M. A. et al. (2012) Phase variable genes of Campylobacter jejuni exhibit high mutation rates and specific mutational patterns but mutability is not the major determinant of population structure during host colonization. Nucleic Acids Res., 40, 5876-5889.
9. Moxon, R., Bayliss, C., Hood, D. (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet., 40, 307-333.
10. Boyer, H. W. (1971) DNA restriction and modification mechanisms in bacteria. Annu. Rev. Microbiol., 25, 153-176.
11. Bujnicki, J. M. (2001) Understanding the evolution of restriction-modification systems: clues from sequence and structure comparisons. Acta Biochim., 48, 935-967.
12. Janulaitis, A., Vaisvila, R., Timinskas, A., Klimasauskas, S., Butkus, V. (1992) Cloning and sequence analysis of the genes coding for Eco57I Type IV restriction-modification enzymes. Nucleic Acids Res., 20, 6051-6056.
13. Shen, B. W., Xu, D., Chan, S. H., Zheng, Y., Zhu, Z., SY, X., Stoddard, B. L. (2011) Characterization and crystal structure of the Type IIG restriction endonuclease RM. BpuSI. Nucl. Acids Res., 39, 8223-8236.
14. Roberts, R. J., Vincze, T., Posfai, J., Macelis, D., (2015) REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nuc. Acids Res., 43, D298-D299.
15. Bickle, T. A., Kruger, D. H. (1993) Biology of DNA restriction. Microbiol. Rev., 57, 434-450.
16. Heusipp, G., Fälker, S., Schmidt, M. A. (2007) DNA adenine methylation and bacterial pathogenesis. Int. J. Med. Microbiol., 297, 1-7.
17. Casadesus, J., Low, D. (2006) Epigenetic gene regulation in the bacterial world. Microbiol. Mol. Biol. Rev., 70, 830-856.
18. Wion, D., Casadesus, J. (2006) N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat. Rev. Microbiol., 4, 183-192.
19. Srikhanta, Y. N., Maguire, T. L., Stacey, K. J., Grimmond, S. M., Jennings, M. P. (2005) The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc. Natl. Acad. Sci. U. S. A., 102, 5547-5551.
20. Srikhanta, Y. N., Dowideit, S. J., Edwards, J. L., Falsetta, M. L., Wu, H. J., Harrison, O. B., Fox, K. L., Seib, K. L., Maguire, T. L., Wang, A. H. et al. (2009) Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog., 5, e1000400.
21. Srikhanta, Y. N., Gorrell, R. J., Steen, J. A., Gawthorne, J. A., Kwok, T. (2011) Phasevarion mediated epigenetic gene regulation in Helicobacter pylori. PLoS One., 6, e27569.
22. Manso, A. S., Chai, M. H., Atack, J. M., Furi, L., De Ste Croix, M., Haigh, R., Trappetti, C., Ogunniyi, A. D., Shewell, L. K., Boitano, M. et al. (2014) A random six-phase switch regulates pneumococcal virulence via global epigenetic changes. Nat. Commun., 5, 5055.
23. Miller, W. G., Pearson, B. M., Wells, J. M., Parker, C. T., Kapitonov, V. V., Mandrell, R. E. (2005) Diversity within the Campylobacter jejuni Type I restriction-modification loci. Microbiology, 151, 337-351.
24. Gardner, S. P., Olson, J. W. (2012) Barriers to horizontal gene transfer in Campylobacter jejuni. Adv. Appl. Microbiol., 79, 19-42.
25. Brathwaite, K. J., Siringan, P., Connerton, P. L., Connerton, I. F. (2015) Host adaption to the bacteriophage carrier state of Campylobacter jejuni. Res. Microbiol., 166, 504-515.
26. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M. et al. (2008) Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res., 36, W465-W469.
27. Sambrook, J., Fritschi, E. F., Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY, USA.
28. Gaskin, D. J. H., Van Vliet, A. H. M., Pearson, B. M. (2007) The Campylobacter genetic toolbox: development of tractable and generally applicable genetic techniques for Campylobacter jejuni. Zoon. Publ. Health., 54, 101.
29. Reeser, R. J., Medler, R. T., Billington, S. J., Jost, B. H., Joens, L. A. (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl. Environ. Microbiol., 73, 1908-1913.
30. Siringan, P., Connerton, P. L., Cummings, N. J., Connerton, I. F. (2014) Alternative bacteriophage life cycles: the carrier state of Campylobacter jejuni. Open Biol., 4, 130200.
31. Atterbury, R. J., Connerton, P. L., Dodd, C. E., Rees, C. E., Connerton, I. F. (2003) Isolation and characterization of Campylobacter bacteriophages from retail poultry. Appl. Environ. Microbiol., 69, 4511-4518.
32. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
33. Baggerly, K., Deng, L., Morris, J., Aldaz, C. (2003) Differential expression in SAGE: accounting for normal between-library variation. Bioinformatics, 19, 1477-1483.
34. Benjamini, Y., Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. B, 57, 289-300.
35. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J., Marra, M. A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res., 19, 1639-1645.
36. Shaw, F. L., Mulholland, F., Le Gall, G., Porcelli, I., Hart, D. J., Pearson, B. M., van Vliet, A. H. (2012) Selenium-dependent biogenesis of formate dehydrogenase in Campylobacter jejuni is controlled by the fdhTU accessory genes. J. Bacteriol., 194, 3814-3823.
37. Murray, I. A., Clark, T. A., Morgan, R. D., Boitano, M., Anton, B. P., Luong, K., Fomenkov, A., Turner, S. W., Korlach, J., Roberts, R. J. (2012) The methylomes of six bacteria. Nucleic Acids Res., 40, 11450-11462.
38. Mou, K. T., Muppirala, U. K., Severin, A. J., Clark, T. A., Boitano, M., Pummer, P. J. (2015) A comparative analysis of methylome profiles of Campylobacter jejuni sheep abortion isolate and gastroenteric strains using PacBio data. Font. Microbiol., 5, 1-15.
39. O'Loughlin, J. L., Eucker, T. P., Chavez, J. D., Samuelson, D. R., Neal-McKinney, J., Gourley, C. R., Bruce, J. E., Konkel, M. E. (2015) Analysis of the Campylobacter jejuni genome by SMRT DNA sequencing identifies restriction-modification motifs. PLoS One, e0118533.
40. Joshua, G. W., Guthrie-Irons, C., Karlyshev, A. V., Wren, B. W. (2006) Biofilm formation in Campylobacter jejuni. Microbiology, 152, 387-396.
41. Srikhanta, Y. N., Fox, K. L., Jennings, M. P. (2010) The phasevarion: phase variation of Type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol., 8, 196-206.
42. Kim, J. S., Li, J., Barnes, I. H., Baltzegar, D. A., Pajaniappan, M., Cullen, T. W., Trent, M. S., Burns, C. M., Thompson, S. A. (2008) Role of the Campylobacter jejuni Cj1461 DNA methyltransferase in regulating virulence characteristics. J. Bacteriol., 190, 6524-6529.
43. Fields, J. A., Thompson, S. A. (2008) Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, host cell invasion. J. Bacteriol., 190, 3411-3416.
44. Leon-Kempis Mdel, R., Guccione, E., Mulholland, F., Williamson, M. P., Kelly, D. J. (2006) The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol. Microbiol., 60, 1262-1275.
45. Pei, Z., Burucoa, C., Grignon, B., Baqar, S., Huang, X.-Z., Kopecko, D. J., Bourgeois, A. L., Fauchere, J.-L., Blaser, M. J. (1998) Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect. Immun., 66, 938-943.
46. Wilson, G. G., Murray, N. E. (1991) Restriction and modification systems. Ann. Rev. Genet., 25, 585-627.
47. Franklin, N. C., Dove, W. F. (1969) Genetic evidence for restriction targets in the DNA of phages lambda and phi 80. Genet. Res., 14, 151-157.
48. Murray, N. E., Manduca De Ritis, P., Foster, L. (1973) DNA targets for the Escherichia coli K restriction system analyzed genetically in recombinants between phages phi80 and lambda. Mol. Gen. Genet., 120, 261-281.
49. Bayliss, C. D., Callaghan, M. J., Moxon, E. R. (2006) High sequence diversity in the mod gene of a phase variable putative type III restriction-modification of Haemophilus influenzae. Nucliec Acids Res., 34, 4046-4059.
50. Jerome, J. P., Bell, J. A., Plovanich-Jones, A. E., Barrick, J. E., Brown, C. T., Mansfield, L. S. (2011) Standing genetic variation in contingency loci drives the rapid host adaptation of Campylobacter jejuni to a novel host. PLoS One, 6, e16399.
51. Goedecke, K., Pignot, M., Goody, R. S., Scheidig, A. J., Weinhold, E. (2001) Structure of the N6-adenine DNA methyltransferase M. TaqI in complex with DNA and a cofactor analog. Nat. Struct. Biol., 8, 121-125.
52. Sails, A. D., Wareing, D. R., Bolton, F. J., Fox, A. J., Curry, A (1998) Characterisation of 16 Campylobacter jejuni and C. coli typing bacteriophages. J. Med. Microbiol., 47, 123-128.
53. Javed, M. A., Ackermann, H. W., Azeredo, J., Carvalho, C. M., Connerton, I., Evoy, S., Hammerl, J. A., Hertwig, S., Lavigne, R., Singh, A. et al. (2014) A suggested classification for two groups of Campylobacter myoviruses. Arch. Virol., 159, 181-190.