Efficient inference of recombination hot regions in bacterial genomes

Molecular Biology and Evolution

Volumn 31, Issue 6, 2014, Pages 1593-1605

  Yahara, Koji ^a,b   Didelot, Xavier ^c   Ansari, M Azim ^d   Sheppard, Samuel K ^b   Falush, Daniel ^e  

^a UNIVERSITY OF TOKYO   (Japan)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

chromosome painting; homologous recombination; population genomics; recombination hot region; recombination hotspot; selection

Indexed keywords

BACTERIAL DNA; MEMBRANE PROTEIN; BACTERIAL PROTEIN;

ALGORITHM; ARTICLE; BACTERIAL GENOME; BACTERIUM ISOLATION; CAMPYLOBACTER JEJUNI; CHROMOSOME PAINTING; CLONAL EVOLUTION; ESCHERICHIA COLI; GENETIC RECOMBINATION; HAPLOTYPE; NONHUMAN; BIOLOGICAL MODEL; BIOLOGY; GENETICS;

ALGORITHMS; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CHROMOSOME PAINTING; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; GENOME, BACTERIAL; MEMBRANE PROTEINS; MODELS, GENETIC; RECOMBINATION, GENETIC;

EID: 84901447428     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu082     Document Type: Article

References (62)

1. Anderson DG, Kowalczykowski SC. 1997. The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a chi-regulated manner. Cell 90:77-86.
2. Auton A, Fledel-Alon A, Pfeifer S, VennO, Ségurel L, Street T, Leffler EM, Bowden R, Aneas I, Broxholme J, et al. 2012. A fine-scale chimpanzee genetic map from population sequencing. Science 336: 193-198.
3. Auton A, McVean G. 2007. Recombination rate estimation in the presence of hotspots. Genome Res. 17:1219-1227.
4. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
5. Browning BL, Browning SR. 2009. A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet. 84: 210-223.
6. Castillo-Ramirez S, Corander J, Marttinen P, Aldeljawi M, Hanage WP, Westh H, Boye K, Gulay Z, Bentley SD, Parkhill J, et al. 2012. Phylogeographic variation in recombination rates within a global clone of methicillin-resistant Staphylococcus aureus. Genome Biol. 13:R126.
7. Chan AH, Jenkins PA, Song YS. 2012. Genome-wide fine-scale recombination rate variation in Drosophila melanogaster. PLoS Genet. 8: e1003090.
8. Cody AJ, Maiden MJ, Dingle KE. 2009. Genetic diversity and stability of the porA allele as a genetic marker in human Campylobacter infection. Microbiology 155:4145-4154.
9. Colles FM, Maiden MC. 2012. Campylobacter sequence typing databases: applications and future prospects. Microbiology 158: 2695-2709.
10. Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM, Parkhill J, Bentley SD, Hanage WP, Lipsitch M. 2013. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet. 45: 656-663.
11. Davis LM, Kakuda T, DiRita VJ. 2009. A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol. 191:1631-1640.
12. Didelot X, Bowden R, Street T, Golubchik T, Spencer C, McVean G, Sangal V, Anjum MF, Achtman M, Falush D, et al. 2011. Recombination and population structure in Salmonella enterica. PLoS Genet. 7:e1002191.
13. Didelot X, Eyre D, Cule M, Ip CL, Ansari M, Griffiths D, Vaughan A, O'Connor L, Golubchik T, Batty E, et al. 2012. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol. 13:R118.
14. Didelot X, Falush D. 2007a. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-1266.
15. Didelot X, Falush D. 2007b. ClonalFrame user guide. [cited 2014 Mar 7]. Available from: http://www.stats.ox.ac.uk/~didelot/files/clonalframe-userguide. pdf.
16. Didelot X, Lawson D, Darling A, Falush D. 2010. Inference of homologous recombination in bacteria using whole-genome sequences. Genetics 186:1435-1449.
17. Didelot X, Lawson D, Falush D. 2009. SimMLST: simulation of multilocus sequence typing data under a neutral model. Bioinformatics 25:1442-1444.
18. Didelot X, Méric G, Falush D, Darling A. 2012. Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genomics 13:256.
19. Dillingham MS, Kowalczykowski SC. 2008. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol Mol Biol Rev. 72: 642-671, table of contents.
20. Frye SA, Nilsen M, Tønjum T, Ambur O. 2013. Dialects of the DNA uptake sequence in Neisseriaceae. PLoS Genet. 9:e1003458.
21. Gaynor EC, Wells D, MacKichan J, Falkow S. 2005. The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol Microbiol. 56:8-27.
22. Guo B, Wang Y, Shi F, Barton Y, Plummer P, Reynolds D, Nettleton D, Grinnage-Pulley T, Lin J, Zhang Q. 2008. CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo. J Bacteriol. 190:1879-1890.
23. Handa N, Yang L, Dillingham M, Kobayashi I, Wigley D, Kowalczykowski S. 2012. Molecular determinants responsible for recognition of the single-stranded DNA regulatory sequence, chi, by RecBCD enzyme. Proc Natl Acad Sci USA. 109:8901-8906.
24. Hein J, Schierup MH, Wiuf C. 2005. Gene genealogies, variation and evolution: a primer in coalescent theory. New York: Oxford University Press.
25. Hinch AG, Tandon A, Patterson N, Song Y, Rohland N, Palmer C, Chen G, Wang K, Buxbaum S, Akylbekova E, et al. 2011. The landscape of recombination in African Americans. Nature 476:170-175.
26. Hudson RR, Kaplan NL. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
27. Hutter S, Vilella A, Rozas J. 2006. Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinformatics 7:409.
28. Jolley KA, Maiden MC. 2010. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595.
29. Joseph SJ, Didelot X, Rothschild J, de Vries H, Morré S, Read T, Dean D. 2012. Population genomics of Chlamydia trachomatis: insights on drift, selection, recombination, and population structure. Mol Biol Evol. 29:3933-3946.
30. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9:286-298.
31. Lawson DJ, Hellenthal G, Myers S, Falush D. 2012. Inference of population structure using dense haplotype data. PLoS Genet. 8:e1002453.
32. Li N, Stephens M. 2003. Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165:2213-2233.
33. Linz B, Schenker M, Zhu P, Achtman M. 2000. Frequent interspecific genetic exchange between commensal Neisseriae and Neisseria meningitidis. Mol Microbiol. 36:1049-1058.
34. Loman NJ, Constantinidou C, Chan J, Halachev M, Sergeant M, Penn C, Robinson E, Pallen M. 2012. High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nat Rev Microbiol. 10:599-606.
35. Marttinen P, Hanage W, Croucher N, Connor T, Harris S, Bentley S, Corander J. 2012. Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res. 40:e6.
36. McVean G, Auton A. 2007. LDhat 2.1: a package for the population genetic analysis of recombination. [cited 2014 Mar 7]. Available from: http://www.stats.ox.ac.uk/~mcvean/LDhat/manual.pdf.
37. McVean G, Awadalla P, Fearnhead P. 2002. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231-1241.
38. McVean GA, Myers S, Hunt S, Deloukas P, Bentley D, Donnelly P. 2004. The fine-scale structure of recombination rate variation in the human genome. Science 304:581-584.
39. Moser I, Schroeder W, Salnikow J. 1997. Campylobacter jejuni major outer membrane protein and a 59-kDa protein are involved in binding to fibronectin and INT 407 cell membranes. FEMS Microbiol Lett. 157:233-238.
40. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. 2005. A fine-scale map of recombination rates and hotspots across the human genome. Science 310:321-324.
41. Namouchi A, Didelot X, Schöck U, Gicquel B, Rocha E. 2012. After the bottleneck: Genome-wide diversification of the Mycobacterium tuberculosis complex by mutation, recombination, and natural selection. Genome Res. 22:721-734.
42. Narra HP, Ochman H. 2006. Of what use is sex to bacteria? Curr Biol 16: R705-R710.
43. Nielsen LN, Luijkx T, Vegge C, Johnsen C, Nuijten P, Wren B, Ingmer H, Krogfelt K. 2011. Identification of immunogenic and virulence-associated Campylobacter jejuni proteins. Clin Vaccine Immunol. 19:113-119.
44. Parker CT, Quinones B,Miller W, Horn S, Mandrell R. 2006. Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J Clin Microbiol. 44:4125-4135.
45. Parkhill J, Wren B, Mungall K, Ketley J, Churcher C, Basham D, Chillingworth T, Davies R, Feltwell T, Holroyd S, et al. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
46. Posada D, Crandall KA. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA. 98:13757-13762.
47. Posada D, Crandall K, Holmes E. 2002. Recombination in evolutionary genomics. Annu Rev Genet. 36:75-97.
48. Price AL, Tandon A, Patterson N, Barnes K, Rafaels N, Ruczinski I, Beaty T, Mathias R, Reich D, Myers S. 2009. Sensitive detection of chromosomal segments of distinct ancestry in admixed populations. PLoS Genet. 5:e1000519.
49. Robinson DR, Foulds LR. 1981. Comparison of phylogenetic trees. Math Biosci. 53:131-147.
50. Rocha EP, Cornet E, Michel B. 2005. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet. 1:e15.
51. Sheppard SK, Didelot X, Jolley KA, Darling AE, Pascoe B, Meric G, Kelly DJ, Cody A, Colles FM, Strachan NJ, et al. 2012. Progressive genomewide introgression in agricultural Campylobacter coli. Mol Ecol. 22: 1051-1064.
52. Sheppard SK, Jolley KA, Maiden MCJ. 2012. A gene-by-gene approach to bacterial population genomics: whole genome MLST of Campylobacter. Genes 3:261-277.
53. Smith JM, Dowson C, Spratt B. 1991. Localized sex in bacteria. Nature 349:29-31.
54. Smith JM, Smith NH, O'Rourke M, Spratt BG. 1993. How clonal are bacteria? Proc Natl Acad Sci USA 90:4384-4388.
55. Takuno S, Kado T, Sugino R, Nakhleh L, Innan H. 2012. Population genomics in bacteria: a case study of Staphylococcus aureus. Mol Biol Evol. 29:797-809.
56. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, et al. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5:e1000344.
57. Treangen TJ, Ambur O, Tonjum T, Rocha E. 2008. The impact of the neisserial DNA uptake sequences on genome evolution and stability. Genome Biol. 9:R60.
58. Vos M, Didelot X. 2009. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 3:199-208.
59. Wilson DJ, Gabriel E, Leatherbarrow A, Cheesbrough J, Gee S, Bolton E, Fox A, Hart C, Diggle P, Fearnhead P. 2009. Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol. 26:385-397.
60. Wiuf C, Hein J. 2000. The coalescent with gene conversion. Genetics 155: 451-462.
61. Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I. 2013. Chromosome painting in silico in a bacterial species reveals fine population structure.Mol Biol Evol. 30: 1454-1464.
62. Yahara K, KawaiM, Furuta Y, Takahashi N, Handa N, Tsuru T, Oshima K, YoshidaM, Azuma T, HattoriM, et al. 2012. Genome-wide survey of mutual homologous recombination in a highly sexual bacterial species. Genome Biol Evol. 4:628-640.