Mobile elements drive recombination hotspots in the core genome of Staphylococcus aureus

Nature Communications

Volumn 5, Issue , 2014, Pages

  Everitt, Richard G ^a,e   Didelot, Xavier ^b,f   Batty, Elizabeth M ^b,c   Miller, Ruth R ^a   Knox, Kyle ^b   Young, Bernadette C ^a   Bowden, Rory ^b,c   Auton, Adam ^c   Votintseva, Antonina ^a,b   Larner Svensson, Hanna ^a,c   Charlesworth, Jane ^a   Golubchik, Tanya ^a,b   Ip, Camilla L C ^b,c   Godwin, Heather ^d   Fung, Rowena ^a   Peto, Tim E A ^a   Walker, A Sarah ^a   Crook, Derrick W ^a   Wilson, Daniel J ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^e UNIVERSITY OF READING   (United Kingdom)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; CHROMOSOME; GENE TRANSFER; GENOME; HOMOLOGY; PATHOGEN; RECOMBINATION;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIUM ISOLATE; GENE MAPPING; GENE TRANSFER; GENOMIC ISLAND; GENOTYPE PHENOTYPE CORRELATION; HOMOLOGOUS RECOMBINATION; HOMOPLASY; NONHUMAN; STAPHYLOCOCCAL CASSETTE CHROMOSOME; STAPHYLOCOCCUS AUREUS; TRANSPOSON; GENE LINKAGE DISEQUILIBRIUM; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; HORIZONTAL GENE TRANSFER; ISOLATION AND PURIFICATION; PHYLOGENY; SPECIES DIFFERENCE; STATISTICAL MODEL;

TRANSPOSON;

CHROMOSOMES, BACTERIAL; DNA TRANSPOSABLE ELEMENTS; GENE TRANSFER, HORIZONTAL; GENETIC VARIATION; GENOME, BACTERIAL; LIKELIHOOD FUNCTIONS; LINKAGE DISEQUILIBRIUM; PHYLOGENY; RECOMBINATION, GENETIC; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS;

EID: 84901447320     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4956     Document Type: Article

References (72)

1. Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304 (2000).
2. Fraser, C., Hanage, W. P. & Spratt, B. G. Recombination and the nature of bacterial speciation. Science 315, 476-480 (2007).
3. Croll, D. & McDonald, B. A. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog. 8, e1002608 (2012).
4. Wright, G. D. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5, 175-186 (2007).
5. MacLean, R. C., Hall, A. R., Perron, G. G. & Buckling, A. The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nat. Rev. Genet. 11, 405-414 (2010).
6. Gordon, N. C. et al. Prediction of Staphylococcus aureus antimicrobial resistance from whole genome sequencing. J. Clin. Microbiol. 52, 1182-1191 (2014).
7. Gerrish, P. J. & Lenski, R. E. The fate of competing beneficial mutations in an asexual population. Genetica 102/103, 127-144 (1998).
8. Pe?rez-Losada, M. et al. Population genetics of microbial pathogens estimated from multilocus sequence typing (MLST) data. Infect. Genet. Evol. 6, 97-112 (2006).
9. Vos, M. & Didelot, X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 3, 199-208 (2009).
10. Thomas, C. M. & Nielsen, K. M. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3, 711-721 (2005).
11. Monk, I. R., Shah, I. M., Xu, M., Tan, M.-W. & Foster, T. J. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3, e00277-e00311 (2012).
12. Lindsay, J. A. & Holden, M. T. G. Understanding the rise and fall of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Funct. Integr. Genomics 6, 186-201 (2006).
13. Harris, S. R. et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327, 469-474 (2010).
14. Castillo-Ramrez, S. et al. Phylogeographic variation in recombination rates within a global clone of methicillin-resistant Staphylococcus aureus. Genome Biol. 13, R126 (2012).
15. Holden, M. T. et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. 23, 653-664 (2013).
16. Strommenger, B. et al. Evolution of methicillin-resistant Staphylococcus aureus towards increasing resistance. J. Antimicrob. Chemother. 69, 616-622 (2013).
17. Kurt, K. et al. Subpopulations of Staphylococcus aureus clonal complex 21 are associated with distinct clinical entities. PLoS ONE 8, e58155 (2013).
18. Miller, R. R. et al. Healthcare-associated outbreak of meticillin-resistant Staphylococcus aureus bacteraemia: role of a cryptic variant of an epidemic clone. J. Hosp. Infect. 86, 83-89 (2014).
19. Wertheim, H. F. et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 5, 751-762 (2005).
20. Cespedes, C. et al. The clonality of Staphylococcus aureus nasal carriage. J. Infect. Dis. 191, 444-452 (2005).
21. Young, B. C. et al. Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc. Natl Acad. Sci. USA 109, 4450-4455 (2012).
22. Golubchik, T. et al. Within-host evolution of Staphylococcus aureus during asymptomatic carriage. PLoS ONE 8, e61319 (2013).
23. Miller, R. R. et al. Dynamics of acquisition and loss of carriage of Staphylococcus aureus strains in the community: the effect of clonal complex. J. Infect. 68, 426-439 (2014).
24. Enright, M. C. et al. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38, 1008-1015 (2000).
25. Holden, M. T. G. et al. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl Acad. Sci. USA 101, 9786-9791 (2004).
26. Gill, S. R. et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187, 2426-2438 (2005).
27. Gillaspy, A. F. et al.in Gram Positive Pathogens. (eds Fischetti, V., Novick, R., Ferretti, J., Portnoy, D. & Rood, J.) 381-412 (ASM Press, 2006).
28. Kuroda, M. et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357, 1225-1240 (2001).
29. Diep, B. A. et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367, 731-739 (2006).
30. Baba, T., Bae, T., Schneewind, O., Takeuchi, F. & Hiramatsu, K. Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J. Bacteriol. 190, 300-310 (2008).
31. Holden, M. T. et al. Genome sequence of a recently emerged, highly transmissible, multi-antibiotic-and antiseptic-resistant variant of methicillinresistant Staphylococcus aureus, sequence type 239 (TW). J. Bacteriol. 192, 888-892 (2010).
32. Schijffelen, M. J., Boel, C. H., van Strijp, J. A. & Fluit, A. C. Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics 11, 376 (2010).
33. Chua, K. et al. Complete genome sequence of Staphylococcus aureus strain JKD6159, a unique Australian clone of ST93-IV community methicillinresistant Staphylococcus aureus. J. Bacteriol. 192, 5556-5557 (2010).
34. Herron-Olson, L., Fitzgerald, J. R., Musser, J. M. & Kapur, V. Molecular correlates of host specialization in Staphylococcus aureus. PLoS ONE 2, e1120 (2007).
35. Guinane, C. M. et al. Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol. Evol. 2, 454-466 (2010).
36. Lowder, B. V. et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc. Natl Acad. Sci. USA 106, 19545-19550 (2009).
37. Hennig, W. Grundzüge einer Theorie der Phylogenetischen Systematik (Deutscher Zentralverlag, 1950).
38. Lankester, E. R. On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreements. Ann. Mag. Nat. Hist. 6, 34-43 (1870).
39. Maynard Smith, J. & Smith, N. H. Detecting recombination from gene trees. Mol. Biol. Evol. 15, 590-599 (1998).
40. Holmes, E. C., Urwin, R. & Maiden, M. C. The influence of recombination on the population structure and evolution of the human pathogen Neisseria meningitidis. Mol. Biol. Evol. 16, 741-749 (1999).
41. Meunier, J. & Eyre-Walker, A. The correlation between linkage disequilibrium and distance: implications for recombination in hominid mitochondria. Mol. Biol. Evol. 18, 2132-2135 (2001).
42. Feil, E. J. et al. How clonal is Staphylococcus aureus? J. Bacteriol. 185, 3307-3316 (2003).
43. Robinson, D. A., Monk, A. B., Cooper, J. E., Feil, E. J. & Enright, M. C. Evolutionary genetics of the accessory gene regulator (agr) locus in Staphylococcus aureus. J. Bacteriol. 187, 8312-8321 (2005).
44. Cooper, J. E. & Feil, E. J. The phylogeny of Staphylococcus aureus-which genes make the best intra-species markers? Microbiology 152, 1297-1305 (2006).
45. McVean, G., Awadalla, P. & Fearnhead, P. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160, 1231-1241 (2002).
46. Didelot, X. & Falush, D. Inference of bacterial microevolution using multilocus sequence data. Genetics 175, 1251-1266 (2007).
47. Robinson, D. A. & Enright, M. C. Evolution of Staphylococcus aureus by large chromosomal replacements. J. Bacteriol. 186, 1060-1064 (2004).
48. Smyth, D. S. & Robinson, D. A. Integrative and sequence characteristics of a novel genetic element, ICE6013, in Staphylococcus aureus. J. Bacteriol. 191, 5964-5975 (2009).
49. Takuno, S., Kado, T., Sugino, R. P., Nakhleh, L. & Innan, H. Population genomics in bacteria: a case study of Staphylococcus aureus. Mol. Biol. Evol. 29, 797-809 (2012).
50. Sung, J. M.-L. & Lindsay, J. A. Staphylococcus aureus strains that are hypersusceptible to resistance gene transfer from enterococci. Antimicrob. Agents Chemother. 51, 2189-2191 (2007).
51. Hanage, W. P., Fraser, C., Tang, J., Connor, T. R. & Corander, J. Hyperrecombination, diversity, and antibiotic resistance in pneumococcus. Science 324, 1454-1457 (2009).
52. Morikawa, K. et al. Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus. PLoS Pathog. 8, e1003003 (2012).
53. Touchon, M. et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5, e1000344 (2009).
54. Flannagan, S. E. & Clewell, D. B. Conjugative transfer of Tn916 in Enterococcus faecalis: transactivation of homologous transposons. J. Bacteriol. 173, 7136-7141 (1991).
55. Hochhut, B., Marrero, J. & Waldor, M. K. Mobilization of plasmids and chromosomal DNA mediated by the SXT element, a constin found in Vibrio cholerae O139. J. Bacteriol. 182, 2043-2047 (2000).
56. Whittle, G., Hamburger, N., Shoemaker, N. B. & Salyers, A. A. A bacteroides conjugative transposon, CTnERL, can transfer a portion of itself by conjugation without excising from the chromosome. J. Bacteriol. 188, 1169-1174 (2006).
57. Brochet, M. et al. Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae. Proc. Natl Acad. Sci. USA 105, 15961-15966 (2008).
58. Brouwer, M. S. M. et al. Horizontal gene transfer converts non-toxigenic Clostridium difficile strains into toxin producers. Nat. Comm. 4, 2601 (2013).
59. Brochet, M. et al. Atypical association of DDE transposition with conjugation specifies a new family of mobile elements. Mol. Microbiol. 71, 948-959 (2009).
60. Lunter, G. & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936-939 (2011).
61. Li, H. et al. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics. 25, 2078-2079 (2009).
62. Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
63. Guindon, S. et al. New algorithms and methods to estimate maximumlikelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010).
64. Pupko, T., Peer, I., Shamir, R. & Graur, D. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 17, 890-896 (2000).
65. Yahara, K., Didelot, X., Ansari, M. A., Sheppard, S. K. & Falush, D. Efficient inference of recombination hot regions in bacterial genomes. Mol. Biol. Evol. (doi:10.1093/molbev/msu082).
66. Goerke, C. et al. Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J. Bacteriol. 191, 3462-3468 (2009).
67. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC). Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob. Agents Chemother. 53, 4961-4967 (2009).
68. Rissman, A. I. et al. Reordering the contigs of draft genomes using the Mauve Aligner. Bioinformatics. 25, 2071-2073 (2009).
69. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/(2013).
70. Tatusov, R. L., Koonin, E. V. & Lipman, D. J. A genomic perspective on protein families. Science 278, 631-637 (1997).
71. Abbott, J. C., Aanensen, D. M., Rutherford, K., Butcher, S. & Spratt, B. G. WebACT-an online companion for the Artemis Comparison Tool. Bioinformatics. 21, 3665-3666 (2005).
72. Guy, L., Kultima, J. R. & Andersson, S. G. GenoPlotR: comparative gene and genome visualization in R. Bioinformatics 26, 2334-2335 (2010).