Use of alignment-free phylogenetics for rapid genome sequence-based typing of helicobacter pylori virulence markers and antibiotic susceptibility

Journal of Clinical Microbiology

Volumn 53, Issue 9, 2015, Pages 2877-2888

  Van Vliet, Arnoud H M ^a   Kusters, Johannes G ^b  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CLARITHROMYCIN; DNA 16S; METRONIDAZOLE; PROTEOME; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIBOSOME PROTEIN; RNA 16S; TETRACYCLINE; ANTIINFECTIVE AGENT; VIRULENCE FACTOR;

ALIGNMENT FREE PHYLOGENETICS; ANTIBIOTIC SENSITIVITY; ARTICLE; BABA2 GENE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BIOINFORMATICS; CAG GENE; CLINICAL GENOMICS; COMPUTER MODEL; CONTROLLED STUDY; DNA BASE COMPOSITION; DUPA GENE; FEATURE FREQUENCY PROFILING PHYLOGENETIC CLUSTERING; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC LINKAGE; GENETIC PROCEDURES; GENOMICS; GENOMOTYPE; GENOTYPE; HELICOBACTER PYLORI; HP918 GENE; ICEA2 GENE; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PATHOGENICITY ISLAND; PHYLOGENETIC TREE; PHYLOGENY; PHYLOGEOGRAPHY; PRIORITY JOURNAL; PZ1 GENE; PZ2 GENE; RNA GENE; SINGLE NUCLEOTIDE POLYMORPHISM; SOUTH AFRICA; VACA GENE; ANTIBIOTIC RESISTANCE; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; EVALUATION STUDY; GENETIC VARIATION; GENETICS; GENOTYPING TECHNIQUE; HUMAN; MOLECULAR TYPING; PROCEDURES;

BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI;

ANTI-BACTERIAL AGENTS; CLUSTER ANALYSIS; DRUG RESISTANCE, BACTERIAL; GENES, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; GENOTYPING TECHNIQUES; HELICOBACTER PYLORI; HUMANS; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; PHYLOGENY; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS;

EID: 84940055814     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.01357-15     Document Type: Article

References (60)

1. Robilotti E, Kamboj M. 2015. Integration of whole-genome sequencing into infection control practices: the potential and the hurdles. J Clin Microbiol 53:1054-1055. http://dx.doi.org/10.1128/JCM.00349-15.
2. Maiden MC, van Rensburg MJ, Bray JE, Earle SG, Ford SA, Jolley KA, McCarthy ND. 2013. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 11:728-736. http://dx.doi.org/10/1038/nrmicro3093.
3. Hedge J, Wilson DJ. 2014. Bacterial phylogenetic reconstruction from whole genomes is robust to recombination but demographic inference is not. mBio 5(6):e02158.
4. Octavia S, Wang Q, Tanaka MM, Kaur S, Sintchenko V, Lan R. 2015. Delineating community outbreaks of Salmonella enterica serovar Typhimurium by use of whole-genome sequencing: insights into genomic variability within an outbreak. J Clin Microbiol 53:1063-1071. http://dx.doi/org/10.1128/JCM.03235-14.
5. Salipante SJ, SenGupta DJ, Cummings LA, Land TA, Hoogestraat DR, Cookson BT. 2015. Application of whole-genome sequencing for bacterial strain typing in molecular epidemiology. J Clin Microbiol 53:1072-1079. http://dx.doi.org/10.1128/JCM.03385-14.
6. Gardner SN, Hall BG. 2013. When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS One 8:e81760. http://dx/doi.org/10.1371/journal.pone.0081760.
7. Bonham-Carter O, Steele J, Bastola D. 2014. Alignment-free genetic sequence comparisons: a review of recent approaches by word analysis. Brief Bioinform 15:890-905. http://dx.doi.org/10.1093/bib/bbt052.
8. Sims GE, Jun SR, Wu GA, Kim SH. 2009. Alignment-free genome comparison with feature frequency profiles (FFP) and optimal resolutions. Proc Natl Acad Sci U S A 106:2677-2682. http://dx.doi.org/10.1073/pnas.0813249106.
9. Sims GE, Kim SH. 2011. Whole-genome phylogeny of Escherichia coli/ Shigella group by feature frequency profiles (FFPs). Proc Natl Acad Sci U S A 108:8329-8334. http://dx.doi.org/10.1073/pnas.1105168108.
10. Cheung MK, Li L, Nong W, Kwan HS. 2011. 2011 German Escherichia coli O104:H4 outbreak: whole-genome phylogeny without alignment. BMC Res Notes 4:533. http://dx.doi.org/10.1186/1756-0500-4-533.
11. Atherton JC, Blaser MJ. 2009. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest 119:2475-2487. http://dx.doi.org/10.1172/JCI38605.
12. Kusters JG, van Vliet AH, Kuipers EJ. 2006. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19:449-490. http://dx.doi.org/10/1128/CMR.00054-05.
13. Graham DY, Fischbach L. 2010. Helicobacter pylori infection. N Engl J Med 363:595-596. http://dx.doi.org/10.1056/NEJMc1006158.
14. Alm RA, Ling LS, Moir DT, King BL, Brown ED, Doig PC, Smith DR, Noonan B, Guild BC, deJonge BL, Carmel G, Tummino PJ, Caruso A, Uria-Nickelsen M, Mills DM, Ives C, Gibson R, Merberg D, Mills SD, Jiang Q, Taylor DE, Vovis GF, Trust TJ. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180. http://dx.doi.org/10.1038/16495.
15. Doig P, de Jonge BL, Alm RA, Brown ED, Uria-Nickelsen M, Noonan B, Mills SD, Tummino P, Carmel G, Guild BC, Moir DT, Vovis GF, Trust TJ. 1999. Helicobacter pylori physiology predicted from genomic comparison of two strains. Microbiol Mol Biol Rev 63:675-707.
16. Didelot X, Nell S, Yang I, Woltemate S, van der Merwe S, Suerbaum S. 2013. Genomic evolution and transmission of Helicobacter pylori in two South African families. Proc Natl Acad Sci U S A 110:13880-13885. http://dx.doi.org/10.1073/pnas.1304681110.
17. Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, Droege M, Reinhardt R, Correa P, Meyer TF, Josenhans C, Falush D, Suerbaum S. 2011. Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci U S A 108:5033-5038. http://dx.doi.org/10.1073/pnas/1018444108.
18. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Megraud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299:1582-1585. http://dx.doi.org/10.1126/science.1080857.
19. Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H, Schlebusch CM, Bernhoft S, Hale J, Suerbaum S, Mugisha L, van der Merwe SW, Achtman M. 2012. Age of the association between Helicobacter pylori and man. PLoS Pathog 8:e1002693. http://dx.doi.org/10.1371/journal/ppat.1002693.
20. van Tonder AJ, Mistry S, Bray JE, Hill DM, Cody AJ, Farmer CL, Klugman KP, von Gottberg A, Bentley SD, Parkhill J, Jolley KA, Maiden MC, Brueggemann AB. 2014. Defining the estimated core genome of bacterial populations using a Bayesian decision model. PLoS Comput Biol 10:e1003788. http://dx.doi.org/10.1371/journal.pc bi.1003788.
21. Fischer W, Windhager L, Rohrer S, Zeiller M, Karnholz A, Hoffmann R, Zimmer R, Haas R. 2010. Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer. Nucleic Acids Res 38:6089-6101. http://dx.doi.org/10.1093/nar/gkq378.
22. Kawai M, Furuta Y, Yahara K, Tsuru T, Oshima K, Handa N, Takahashi N, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I. 2011. Evolution in an oncogenic bacterial species with extreme genome plasticity: Helicobacter pylori East Asian genomes. BMC Microbiol 11:104. http://dx.doi.org/10.1186/1471-2180-11-104.
23. Jun SR, Sims GE, Wu GA, Kim SH. 2010. Whole-proteome phylogeny of prokaryotes by feature frequency profiles: an alignment-free method with optimal feature resolution. Proc Natl Acad Sci U S A 107:133-138. http://dx.doi.org/10.1073/pnas.0913033107.
24. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, Gillespie JJ, Gough R, Hix D, Kenyon R, Machi D, Mao C, Nordberg EK, Olson R, Overbeek R, Pusch GD, Shukla M, Schulman J, Stevens RL, Sullivan DE, Vonstein V, Warren A, Will R, Wilson MJ, Yoo HS, Zhang C, Zhang Y, Sobral BW. 2014. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 42:D581-591. http://dx.doi.org/10.1093/nar/gkt1099.
25. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi/org/10.1101/gr.074492.107.
26. Field D, Tiwari B, Booth T, Houten S, Swan D, Bertrand N, Thurston M. 2006. Open software for biologists: from famine to feast. Nat Biotechnol 24:801-803. http://dx.doi.org/10.1038/nbt0706-801.
27. Felsenstein J. 1989. PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164-166.
28. Marais G, Kingsford C. 2011. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764-770. http://dx.doi.org/10.1093/bioinformatics/btr011.
29. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. http://dx/doi.org/10.1371/journal.pone.0009490.
30. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. 2004. Versatile and open software for comparing large genomes. Genome Biol 5:R12. http://dx.doi.org/10.1186/gb-2004-5-2-r12.
31. Hysom DA, Naraghi-Arani P, Elsheikh M, Carrillo AC, Williams PL, Gardner SN. 2012. Skip the alignment: degenerate, multiplex primer and probe design using K-mer matching instead of alignments. PLoS One 7:e34560. http://dx.doi.org/10.1371/journal.pone.0034560.
32. Treangen TJ, Ondov BD, Koren S, Phillippy AM. 2014. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15:524. http://dx.doi.org/10.1186/s13059-014-0524-x.
33. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
35. Kruczkiewicz P, Mutschall S, Barker D, Thomas J, Van Domselaar G, Gannon VPJ, Carrillo CD, Taboada EN. 2013. MIST: a tool for rapid in silico generation of molecular data from bacterial genome sequences. Bioinformatics 2013:316-323.
36. Armitano RI, Matteo MJ, Goldman C, Wonaga A, Viola LA, De Palma GZ, Catalano M. 2013. Helicobacter pylori heterogeneity in patients with gastritis and peptic ulcer disease. Infect Genet Evol 16:377-385. http://dx/doi.org/10.1016/j.meegid.2013.02.024.
37. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547. http://dx.doi/org/10.1038/41483.
38. Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, Haas R. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol 42:1337-1348.
39. Johnson EM, Gaddy JA, Voss BJ, Hennig EE, Cover TL. 2014. Genes required for assembly of pili associated with the Helicobacter pylori cag type IV secretion system. Infect Immun 82:3457-3470. http://dx.doi.org/10.1128/IAI.01640-14.
40. Goodwin A, Kersulyte D, Sisson G, Veldhuyzen van Zanten SJ, Berg DE, Hoffman PS. 1998. Metronidazole resistance in Helicobacter pylori is due to null mutations in a gene (rdxA) that encodes an oxygen-insensitive NADPH nitroreductase. Mol Microbiol 28:383-393. http://dx.doi.org/10/1046/j.1365-2958.1998.00806.x.
41. Kwon DH, El-Zaatari FA, Kato M, Osato MS, Reddy R, Yamaoka Y, Graham DY. 2000. Analysis of rdxA and involvement of additional genes encoding NAD(P)H flavin oxidoreductase (FrxA) and ferredoxin-like protein (FdxB) in metronidazole resistance of Helicobacter pylori. Antimicrob Agents Chemother 44:2133-2142. http://dx.doi.org/10.1128/AAC/44.8.2133-2142.2000.
42. Gerrits MM, Berning M, Van Vliet AH, Kuipers EJ, Kusters JG. 2003. Effects of 16S rRNA gene mutations on tetracycline resistance in Helicobacter pylori. Antimicrob Agents Chemother 47:2984-2986. http://dx.doi/org/10.1128/AAC.47.9.2984-2986.2003.
43. Teh X, Khosravi Y, Lee WC, Leow AH, Loke MF, Vadivelu J, Goh KL. 2014. Functional and molecular surveillance of Helicobacter pylori antibiotic resistance in Kuala Lumpur. PLoS One 9:e101481. http://dx.doi.org/10.1371/journal.pone.0101481.
44. Tankovic J, Lascols C, Sculo Q, Petit JC, Soussy CJ. 2003. Single and double mutations in gyrA but not in gyrB are associated with low-and high-level fluoroquinolone resistance in Helicobacter pylori. Antimicrob Agents Chemother 47:3942-3944. http://dx.doi.org/10.1128/AAC.47.12/3942-3944.2003.
45. 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. http://dx.doi.org/10.1093/molbev/mst055.
46. Lu W, Wise MJ, Tay CY, Windsor HM, Marshall BJ, Peacock C, Perkins T. 2014. Comparative analysis of the full genome of Helicobacter pylori isolate Sahul64 identifies genes of high divergence. J Bacteriol 196:1073-1083. http://dx.doi.org/10.1128/JB.01021-13.
47. Maldonado-Contreras A, Mane SP, Zhang XS, Pericchi L, Alarcon T, Contreras M, Linz B, Blaser MJ, Dominguez-Bello MG. 2013. Phylogeographic evidence of cognate recognition site patterns and transformation efficiency differences in H. pylori: theory of strain dominance. BMC Microbiol 13:211. http://dx.doi.org/10.1186/1471-2180-13-211.
48. Atherton JC, Cover TL, Twells RJ, Morales MR, Hawkey CJ, Blaser MJ. 1999. Simple and accurate PCR-based system for typing vacuolating cytotoxin alleles of Helicobacter pylori. J Clin Microbiol 37:2979-2982.
49. Mizushima T, Sugiyama T, Komatsu Y, Ishizuka J, Kato M, Asaka M. 2001. Clinical relevance of the babA2 genotype of Helicobacter pylori in Japanese clinical isolates. J Clin Microbiol 39:2463-2465. http://dx.doi/org/10.1128/JCM.39.7.2463-2465.2001.
50. Yamaoka, Y. 2012. Pathogenesis of Helicobacter pylori-related gastroduodenal diseases from molecular epidemiological studies. Gastroenterol Res Pract 2012:371503.
51. Gerrits MM, van Vliet AH, Kuipers EJ, Kusters JG. 2006. Helicobacter pylori and antimicrobial resistance: molecular mechanisms and clinical implications. Lancet Infect Dis 6:699-709. http://dx.doi.org/10.1016/S1473-3099(06)70627-2.
52. Khan R, Nahar S, Sultana J, Ahmad MM, Rahman M. 2004. T2182C mutation in 23S rRNA is associated with clarithromycin resistance in Helicobacter pylori isolates obtained in Bangladesh. Antimicrob Agents Chemother 48:3567-3569. http://dx.doi.org/10.1128/AAC.48.9.3567/3569.2004.
53. Kaakoush NO, Asencio C, Megraud F, Mendz GL. 2009. A redox basis for metronidazole resistance in Helicobacter pylori. Antimicrob Agents Chemother 53:1884-1891. http://dx.doi.org/10.1128/AAC.01449-08.
54. Gerrits MM, de Zoete MR, Arents NL, Kuipers EJ, Kusters JG. 2002. 16S rRNA mutation-mediated tetracycline resistance in Helicobacter pylori. Antimicrob Agents Chemother 46:2996-3000. http://dx.doi.org/10.1128/AAC.46.9.2996-3000.2002.
55. Trieber CA, Taylor DE. 2002. Mutations in the 16S rRNA genes of Helicobacter pylori mediate resistance to tetracycline. J Bacteriol 184:2131-2140. http://dx.doi.org/10.1128/JB.184.8.2131-2140.2002.
56. Land M, Hauser L, Jun SR, Nookaew I, Leuze MR, Ahn TH, Karpinets T, Lund O, Kora G, Wassenaar T, Poudel S, Ussery DW. 2015. Insights from 20 years of bacterial genome sequencing. Funct Integr Genomics 15:141-161. http://dx.doi.org/10.1007/s10142-015-0433-4.
57. Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, Yamaoka Y, Graham DY, Perez-Trallero E, Wadstrom T, Suerbaum S, Achtman M. 2007. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445:915-918. http://dx.doi.org/10.1038/nature05562.
58. Kumar N, Mariappan V, Baddam R, Lankapalli AK, Shaik S, Goh KL, Loke MF, Perkins T, Benghezal M, Hasnain SE, Vadivelu J, Marshall BJ, Ahmed N. 2015. Comparative genomic analysis of Helicobacter pylori from Malaysia identifies three distinct lineages suggestive of differential evolution. Nucleic Acids Res 43:324-335. http://dx.doi.org/10.1093/nar/gku1271.
59. Rehvathy V, Tan MH, Gunaletchumy SP, Teh X, Wang S, Baybayan P, Singh S, Ashby M, Kaakoush NO, Mitchell HM, Croft LJ, Goh KL, Loke MF, Vadivelu J. 2013. Multiple genome sequences of Helicobacter pylori strains of diverse disease and antibiotic resistance backgrounds from Malaysia. Genome Announc 1(5):e00687-13.
60. Burucoa C, Landron C, Garnier M, Fauchere JL. 2005. T2182C mutation is not associated with clarithromycin resistance in Helicobacter pylori. Antimicrob Agents Chemother 49:868. (Author reply, 49:868-870.) http://dx.doi.org/10.1128/AAC.49.2.868-870.2005.