Genome-wide survey of codons under diversifying selection in a highly recombining bacterial species, Helicobacter pylori

DNA Research

Volumn 23, Issue 2, 2016, Pages 135-143

  Yahara, Koji ^a,b,c   Furuta, Yoshikazu ^c   Morimoto, Shinpei ^d   Kikutake, Chie ^d   Komukai, Sho ^d   Matelska, Dorota ^e   Dunin Horkawicz, Stanisław ^e   Bujnicki, Janusz M ^e,f   Uchiyama, Ikuo ^g   Kobayashi, Ichizo ^c  

^a KURUME UNIVERSITY   (Japan)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF TOKYO   (Japan)

^d KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^f ADAM MICKIEWICZ UNIVERSITY   (Poland)

^g NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

bacteria; dN dS; population genomics; recombination; selection

Indexed keywords

AMINO ACID; NUCLEOTIDE; CODON;

ARTICLE; BACTERIAL GENOME; CODON; CONTROLLED STUDY; DIVERSIFYING SELECTION; DNA MODIFICATION; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; HELICOBACTER PYLORI; HOMOLOGOUS RECOMBINATION; NONHUMAN; PROTEIN STRUCTURE; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION;

CODON; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, BACTERIAL; HELICOBACTER PYLORI; RECOMBINATION, GENETIC; SELECTION, GENETIC;

EID: 84965144138     PISSN: 13402838     EISSN: 17561663     Source Type: Journal    
DOI: 10.1093/dnares/dsw003     Document Type: Article

References (64)

1. Sabeti, P.C., Schaffner, S.F., Fry, B., et al. 2006, Positive natural selection in the human lineage, Science, 312, 1614-20.
2. Karlsson, E.K., Kwiatkowski, D.P. and Sabeti, P.C. 2014, Natural selection and infectious disease in human populations, Nat. Rev. Genet., 15, 379-93.
3. Kosiol, C. and Anisimova, M. 2012, Selection on the protein-coding genome, In:Anisimova, M. (ed.), Evolutionary Genomics. Humana Press, c/o Springer Science + Business Media: New York, pp. 113-40.
4. Shapiro, B.J. and Alm, E.J. 2008, Comparing patterns of natural selection across species using selective signatures, PLoS Genet., 4, e23.
5. Lefebure, T. and Stanhope, M.J. 2007, Evolution of the core and pangenome of Streptococcus: positive selection, recombination, and genome composition, Genome Biol., 8, R71.
6. Olbermann, P., Josenhans, C., Moodley, Y., et al. 2010, A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island, PLoS Genet., 6, e1001069.
7. Petersen, L., Bollback, J.P., Dimmic, M., Hubisz, M. and Nielsen, R. 2007, Genes under positive selection in Escherichia coli, Genome Res., 17, 1336-43.
8. Anisimova, M., Nielsen, R. and Yang, Z. 2003, Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites, Genetics, 164, 1229-36.
9. Shriner, D., Nickle, D.C., Jensen, M.A. and Mullins, J.I. 2003, Potential impact of recombination on sitewise approaches for detecting positive natural selection, Genet. Res., 81, 115-21.
10. Su, F., Ou, H.Y., Tao, F., Tang, H. and Xu, P. 2013, PSP: rapid identification of orthologous coding genes under positive selection across multiple closely related prokaryotic genomes, BMC Genomics, 14, 924.
11. Wilson, D.J. and McVean, G. 2006, Estimating diversifying selection and functional constraint in the presence of recombination, Genetics, 172, 1411-25.
12. Didelot, X., Bowden, R., Wilson, D.J., Peto, T.E. and Crook, D.W. 2012, Transforming clinical microbiology with bacterial genome sequencing, Nat. Rev. Genet., 13, 601-12.
13. Suerbaum, S. and Josenhans, C. 2007, Helicobacter pylori evolution and phenotypic diversification in a changing host, Nat. Rev. Microbiol., 5, 441-52.
14. Kennemann, L., Didelot, X., Aebischer, T., et al. 2011, Helicobacter pylori genome evolution during human infection, Proc. Natl. Acad. Sci. USA, 108, 5033-8.
15. Yahara, K., Didelot, X., Ansari, M.A., Sheppard, S.K. and Falush, D. 2014, Efficient inference of recombination hot regions in bacterial genomes, Mol. Biol. Evol., 31, 1593-605.
16. Yahara, K., Furuta, Y., Oshima, K., et al. 2013, Chromosome painting in silico in a bacterial species reveals fine population structure, Mol. Biol. Evol., 30, 1454-64.
17. Uchiyama, I. 2006, Hierarchical clustering algorithm for comprehensive orthologous-domain classification in multiple genomes, Nucleic Acids Res., 34, 647-58.
18. Kosiol, C., Holmes, I. and Goldman, N. 2007, An empirical codon model for protein sequence evolution, Mol. Biol. Evol., 24, 1464-79.
19. Loytynoja, A. and Goldman, N. 2008, Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis, Science, 320, 1632-5.
20. Jordan, G. and Goldman, N. 2012, The effects of alignment error and alignment filtering on the sitewise detection of positive selection, Mol. Biol. Evol., 29, 1125-39.
21. Fletcher, W. and Yang, Z. 2010, The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection, Mol. Biol. Evol., 27, 2257-67.
22. Gelman, A. and Rubin, D.B. 1992, Inference from iterative simulation using multiple sequences, Stat. Sci., 7, 457-511.
23. Congdon, P.D. 2010, Applied Bayesian Hierarchical Methods. Chapman and Hall/CRC: Boca Raton, FL.
24. Brooks, S.P. and Gelman, A. 1998, General methods for monitoring convergence of iterative simulations, J. Comput. Graph. Stat., 7, 434-55.
25. Plummer, M., Best, N., Cowles, K. and Vines, K. 2006, CODA: convergence diagnosis and output analysis for MCMC, R News, 6, 7-11.
26. Dondelinger, F., Lèbre, S. and Husmeier, D. 2013, Non-homogeneous dynamic Bayesian networks with Bayesian regularization for inferring gene regulatory networks with gradually time-varying structure, Mach. Learn., 90, 191-230.
27. Uchiyama, I., Mihara, M., Nishide, H. and Chiba, H. 2014, MBGD update 2015: microbial genome database for flexible ortholog analysis utilizing a diverse set of genomic data, Nucleic Acids Res., 43, D270-6.
28. Uchiyama, I. 2003, MBGD: microbial genome database for comparative analysis, Nucleic Acids Res., 31, 58-62.
29. Kurowski, M.A. and Bujnicki, J.M. 2003, GeneSilico protein structure prediction meta-server, Nucleic Acids Res., 31, 3305-7.
30. Kosinski, J., Cymerman, I.A., Feder, M., Kurowski, M.A., Sasin, J.M. and Bujnicki, J.M. 2003, A 'FRankenstein's monster' approach to comparative modeling: merging the finest fragments of Fold-Recognition models and iterative model refinement aided by 3D structure evaluation, Proteins, 53 (Suppl 6), 369-79.
31. Kosinski, J., Gajda, M.J., Cymerman, I.A., et al. 2005, FRankenstein becomes a cyborg: the automatic recombination and realignment of fold recognition models in CASP6, Proteins, 61(Suppl 7), 106-13.
32. Sali, A. and Blundell, T.L. 1993, Comparative protein modelling by satisfaction of spatial restraints, J. Mol. Biol., 234, 779-815.
33. Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J. and Schwede, T. 2009, Protein structure homology modeling using SWISS-MODEL workspace, Nat. Protoc., 4, 1-13.
34. Berman, H.M., Westbrook, J., Feng, Z., et al. 2000, The Protein Data Bank, Nucleic Acids Res., 28, 235-42.
35. Hutter, S., Vilella, A.J. and Rozas, J. 2006, Genome-wide DNA polymorphism analyses using VariScan, BMC Bioinformatics, 7, 409.
36. Yahara, K., Didelot, X., Jolley, K.A., et al. in press, The landscape of realized homologous recombination in pathogenic bacteria, Mol. Biol. Evol., 33, 456-71.
37. Grizot, S., Salem, M., Vongsouthi, V., et al. 2006, Structure of the Escherichia coli heptosyltransferase WaaC: binary complexes with ADP and ADP-2-deoxy-2-fluoro heptose, J. Mol. Biol., 363, 383-94.
38. Chaput, C., Ecobichon, C., Cayet, N., et al. 2006, Role of AmiA in the morphological transition of Helicobacter pylori and in immune escape, PLoS Pathog., 2, e97.
39. Cerda, O., Rivas, A. and Toledo, H. 2003, Helicobacter pylori strain ATCC700392 encodes a methyl-accepting chemotaxis receptor protein (MCP) for arginine and sodium bicarbonate, FEMS Microbiol. Lett., 224, 175-81.
40. Amundsen, S.K., Fero, J., Hansen, L.M., et al. 2008, Helicobacter pylori AddAB helicase-nuclease and RecA promote recombination-related DNA repair and survival during stomach colonization, Mol. Microbiol., 69, 994-1007.
41. Handa, N., Yang, L., Dillingham, M.S., Kobayashi, I., Wigley, D.B. and Kowalczykowski, S.C. 2012, Molecular determinants responsible for recognition of the single-stranded DNA regulatory sequence, chi, by RecBCD enzyme, Proc. Natl. Acad. Sci. USA, 109, 8901-6.
42. Kawai, M., Furuta, Y., Yahara, K., et al. 2011, Evolution in an oncogenic bacterial species with extreme genome plasticity: Helicobacter pylori East Asian genomes, BMC Microbiol., 11, 104.
43. Singleton, M.R., Dillingham, M.S., Gaudier, M., Kowalczykowski, S.C. and Wigley, D.B. 2004, Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks, Nature, 432, 187-93.
44. Furuta, Y. and Kobayashi, I. 2013, Restriction-modification systems as mobile epigenetic elements, In:Roberts, A. and Mullany, P. (eds.), Bacterial Integrative Mobile Genetic Elements, Landes Bioscience, Austin, Texas, pp. 85-103.
45. Nobusato, A., Uchiyama, I. and Kobayashi, I. 2000, Diversity of restriction-modification gene homologues in Helicobacter pylori, Gene, 259, 89-98.
46. Lin, L.F., Posfai, J., Roberts, R.J. and Kong, H. 2001, Comparative genomics of the restriction-modification systems in Helicobacter pylori, Proc. Natl. Acad. Sci. USA, 98, 2740-5.
47. Kong, H., Lin, L.F., Porter, N., et al. 2000, Functional analysis of putative restriction-modification system genes in the Helicobacter pylori J99 genome, Nucleic Acids Res., 28, 3216-23.
48. Lapkouski, M., Panjikar, S., Janscak, P., et al. 2009, Structure of the motor subunit of type I restriction-modification complex EcoR124I, Nat. Struct. Mol. Biol., 16, 94-5.
49. Obarska, A., Blundell, A., Feder, M., et al. 2006, Structural model for the multisubunit Type IC restriction-modification DNA methyltransferase M. EcoR124I in complex with DNA, Nucleic Acids Res., 34, 1992-2005.
50. Bickle, T.A. and Kruger, D.H. 1993, Biology of DNA restriction, Microbiol. Rev., 57, 434-50.
51. Kim, J.S., DeGiovanni, A., Jancarik, J., et al. 2005, Crystal structure of DNA sequence specificity subunit of a type I restriction-modification enzyme and its functional implications, Proc.Natl.Acad.Sci.USA, 102, 3248-53.
52. Price, C., Lingner, J., Bickle, T.A., Firman, K. and Glover, S.W. 1989, Basis for changes in DNA recognition by the EcoR124 and EcoR124/3 type I DNA restriction and modification enzymes, J. Mol. Biol., 205, 115-25.
53. Sharma, C.M., Hoffmann, S., Darfeuille, F., et al. 2010, The primary transcriptome of the major human pathogen Helicobacter pylori, Nature, 464, 250-5.
54. Furuta, Y., Yahara, K., Hatakeyama, M. and Kobayashi, I. 2011, Evolution of cagA oncogene of Helicobacter pylori through recombination, PLoS One, 6, e23499.
55. Elgrably-Weiss, M., Park, S., Schlosser-Silverman, E., Rosenshine, I., Imlay, J. and Altuvia, S. 2002, A Salmonella enterica serovar typhimurium hemA mutant is highly susceptible to oxidative DNA damage, J. Bacteriol., 184, 3774-84.
56. Kennemann, L., Brenneke, B., Andres, S., et al. 2012, In vivo sequence variation in HopZ, a phase-variable outer membrane protein of Helicobacter pylori, Infect. Immun., 80, 4364-73.
57. Kobayashi, I. 2001, Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution, Nucleic Acids Res., 29, 3742-56.
58. Furuta, Y., Namba-Fukuyo, H., Shibata, T.F., et al. 2014, Methylome diversification through changes in DNA methyltransferase sequence specificity, PLoS Genet., 10, e1004272.
59. Mruk, I. and Kobayashi, I. 2014, To be or not to be: regulation of restriction-modification systems and other toxin-antitoxin systems, Nucleic Acids Res., 42, 70-86.
60. Montano, V., Didelot, X., Foll, M., et al. 2015, Worldwide population structure, long-term demography, and local adaptation of Helicobacter pylori, Genetics, 200, 947-63.
61. Michod, R.E. and Levin, B.R. 1988, The Evolution of Sex: An Examination of Current Ideas. Sinauer: Sunderland, MA.
62. Hamilton, W.D. 1990, Sexual reproduction as an adaptation to resist parasites (a review), Proc. Natl. Acad. Sci. USA, 87, 3566-73.
63. Joseph, S.J., Didelot, X., Gandhi, K., Dean, D. and Read, T.D. 2011, Interplay of recombination and selection in the genomes of Chlamydia trachomatis, Biol. Direct., 6, 28.
64. Orsi, R.H., Sun, Q. and Wiedmann, M. 2008, Genome-wide analyses reveal lineage specific contributions of positive selection and recombination to the evolution of Listeria monocytogenes, BMC Evol. Biol., 8, 233.