Bidirectional genomic exchange between Helicobacter pylori strains from a family in Coventry, United Kingdom

International Journal of Medical Microbiology

Volumn 304, Issue 8, 2014, Pages 1135-1146

  Krebes, Juliane ^a,b   Didelot, Xavier ^c   Kennemann, Lynn ^a   Suerbaum, Sebastian ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Center for Experimental and Clinical Infection Research   (Germany)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

454 sequencing; Genome evolution; Helicobacter pylori; Mutation; Recombination; Transmission

Indexed keywords

DNA; GENOMIC DNA; OUTER MEMBRANE PROTEIN; BACTERIAL DNA;

ADULT; AGED; ARTICLE; BACTERIAL STRAIN; BACTERIUM TRANSFORMATION; CLINICAL ARTICLE; GENE; GENE FREQUENCY; GENE SEQUENCE; GENETIC CODE; GENETIC DISTANCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOMOLOGOUS RECOMBINATION; HUMAN; IN VITRO STUDY; MIXED INFECTION; MOLECULAR PHYLOGENY; MUTATION RATE; NONHUMAN; PATHOGENICITY ISLAND; SINGLE NUCLEOTIDE POLYMORPHISM; SPONTANEOUS MUTATION; UNITED KINGDOM; ADOLESCENT; BACTERIAL GENOME; CASE REPORT; CHEMISTRY; DNA SEQUENCE; FAMILY HEALTH; GENETICS; GENOTYPE; HORIZONTAL GENE TRANSFER; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; MIDDLE AGED; MOLECULAR GENETICS;

ADOLESCENT; AGED; DNA, BACTERIAL; FAMILY HEALTH; GENE TRANSFER, HORIZONTAL; GENETIC VARIATION; GENOME, BACTERIAL; GENOTYPE; GREAT BRITAIN; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84912033016     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.08.007     Document Type: Article

References (41)

1. Alm R.A., Bina J., Andrews B.M., Doig P., Hancock R.E., Trust T.J. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect. Immun. 2000, 68:4155-4168.
2. Alm R.A., Ling L.S., Moir D.T., King B.L., Brown E.D., Doig P.C., Smith D.R., Noonan B., Guild B.C., deJonge B.L., Carmel G., Tummino P.J., Caruso A., Uria-Nickelsen M., Mills D.M., Ives C., Gibson R., Merberg D., Mills S.D., Jiang Q., Taylor D.E., Vovis G.F., Trust T.J. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999, 397:176-180.
3. Aziz R.K., Bartels D., Best A.A., DeJongh M., Disz T., Edwards R.A., Formsma K., Gerdes S., Glass E.M., Kubal M., Meyer F., Olsen G.J., Olson R., Osterman A.L., Overbeek R.A., McNeil L.K., Paarmann D., Paczian T., Parrello B., Pusch G.D., Reich C., Stevens R., Vassieva O., Vonstein V., Wilke A., Zagnitko O. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75.
4. Bjorkholm B., Sjolund M., Falk P.G., Berg O.G., Engstrand L., Andersson D.I. Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:14607-14612.
5. Carver T., Thomson N., Bleasby A., Berriman M., Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009, 25:119-120.
6. Didelot X., Achtman M., Parkhill J., Thomson N.R., Falush D. A bimodal pattern of relatedness between the Salmonella paratyphi A and typhi genomes: convergence or divergence by homologous recombination?. Genome Res. 2007, 17:61-68.
7. Didelot X., Nell S., Yang I., Woltemate S., van der M.S., Suerbaum S. Genomic evolution and transmission of Helicobacter pylori in two South African families. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:13880-13885.
8. Falush D., Kraft C., Taylor N.S., Correa P., Fox J.G., Achtman M., Suerbaum S. Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:15056-15061.
9. Falush D., Wirth T., Linz B., Pritchard J.K., Stephens M., Kidd M., Blaser M.J., Graham D.Y., Vacher S., Perez-Perez G.I., Yamaoka Y., Megraud F., Otto K., Reichard U., Katzowitsch E., Wang X., Achtman M., Suerbaum S. Traces of human migrations in Helicobacter pylori populations. Science 2003, 299:1582-1585.
10. Frenck R.W., Clemens J. Helicobacter in the developing world. Microbes. Infect. 2003, 5:705-713.
11. Guisset M., Coton T., Rey P., Debonne J.M. Helicobacter pylori infection in developing countries. Med. Trop. (Mars.) 1997, 57:77-82.
12. Hofreuter D., Odenbreit S., Haas R. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 2001, 41:379-391.
13. Horst J.P., Wu T.H., Marinus M.G. Escherichia coli mutator genes. Trends Microbiol. 1999, 7:29-36.
14. Ilver D., Arnqvist A., Ogren J., Frick I.M., Kersulyte D., Incecik E.T., Berg D.E., Covacci A., Engstrand L., Boren T. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998, 279:373-377.
15. Kennemann L., Didelot X., Aebischer T., Kuhn S., Drescher B., Droege M., Reinhardt R., Correa P., Meyer T.F., Josenhans C., Falush D., Suerbaum S. Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5033-5038.
16. Kersulyte D., Chalkauskas H., Berg D.E. Emergence of recombinant strains of Helicobacter pylori during human infection. Mol. Microbiol. 1999, 31:31-43.
17. Kulick S., Moccia C., Didelot X., Falush D., Kraft C., Suerbaum S. Mosaic DNA imports with interspersions of recipient sequence after natural transformation of Helicobacter pylori. PLoS ONE 2008, 3:e3797.
18. Kurtz S., Phillippy A., Delcher A.L., Smoot M., Shumway M., Antonescu C., Salzberg S.L. Versatile and open software for comparing large genomes. Genome Biol. 2004, 5:R12.
19. Lin E.A., Zhang X.S., Levine S.M., Gill S.R., Falush D., Blaser M.J. Natural transformation of Helicobacter pylori involves the integration of short DNA fragments interrupted by gaps of variable size. PLoS Pathog. 2009, 5:e1000337.
20. Linz B., Balloux F., Moodley Y., Manica A., Liu H., Roumagnac P., Falush D., Stamer C., Prugnolle F., van der Merwe S.W., Yamaoka Y., Graham D.Y., Perez-Trallero E., Wadstrom T., Suerbaum S., Achtman M. An African origin for the intimate association between humans and Helicobacter pylori. Nature 2007, 445:915-918.
21. Linz B., Windsor H.M., Gajewski J.P., Hake C.M., Drautz D.I., Schuster S.C., Marshall B.J. Helicobacter pylori genomic microevolution during naturally occurring transmission between adults. PLOS ONE 2013, 8:e82187.
22. Lundin A., Bjorkholm B., Kupershmidt I., Unemo M., Nilsson P., Andersson D.I., Engstrand L. Slow genetic divergence of Helicobacter pylori strains during long-term colonization. Infect. Immun. 2005, 73:4818-4822.
23. Mahdavi J., Sonden B., Hurtig M., Olfat F.O., Forsberg L., Roche N., Angstrom J., Larsson T., Teneberg S., Karlsson K.A., Altraja S., Wadstrom T., Kersulyte D., Berg D.E., Dubois A., Petersson C., Magnusson K.E., Norberg T., Lindh F., Lundskog B.B., Arnqvist A., Hammarstrom L., Boren T. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002, 297:573-578.
24. Miller J.H. Mutators in Escherichia coli. Mutat. Res. 1998, 409:99-106.
25. Moccia C., Krebes J., Kulick S., Didelot X., Kraft C., Bahlawane C., Suerbaum S. The nucleotide excision repair (NER) system of Helicobacter pylori: role in mutation prevention and chromosomal import patterns after natural transformation. BMC Microbiol. 2012, 12:67.
26. Moodley Y., Linz B., Bond R.P., Nieuwoudt M., Soodyall H., Schlebusch C.M., Bernhoft S., Hale J., Suerbaum S., Mugisha L., van der Merwe S.W., Achtman M. Age of the association between Helicobacter pylori and man. PLoS Pathog. 2012, 8:e1002693.
27. Moodley Y., Linz B., Yamaoka Y., Windsor H.M., Breurec S., Wu J.Y., Maady A., Bernhoft S., Thiberge J.M., Phuanukoonnon S., Jobb G., Siba P., Graham D.Y., Marshall B.J., Achtman M. The peopling of the Pacific from a bacterial perspective. Science 2009, 323:527-530.
28. Morelli G., Didelot X., Kusecek B., Schwarz S., Bahlawane C., Falush D., Suerbaum S., Achtman M. Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet. 2010, 6:e1001036.
29. Nwokolo C.U., Bickley J., Attard A.R., Owen R.J., Costas M., Fraser I.A. Evidence of clonal variants of Helicobacter pylori in three generations of a duodenal ulcer disease family. Gut 1992, 33:1323-1327.
30. Odenbreit S., Faller G., Haas R. Role of the AlpAB proteins and lipopolysaccharide in adhesion of Helicobacter pylori to human gastric tissue. Int. J. Med. Microbiol. 2002, 292:247-256.
31. Odenbreit S., Till M., Hofreuter D., Faller G., Haas R. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 1999, 31:1537-1548.
32. Owen R.J., Xerry J. Tracing clonality of Helicobacter pylori infecting family members from analysis of DNA sequences of three housekeeping genes (ureI, atpA and ahpC), deduced amino acid sequences, and pathogenicity-associated markers (cagA and vacA). J. Med. Microbiol. 2003, 52:515-524.
33. Peck B., Ortkamp M., Diehl K.D., Hundt E., Knapp B. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucleic Acids Res. 1999, 27:3325-3333.
34. Schwarz S., Morelli G., Kusecek B., Manica A., Balloux F., Owen R.J., Graham D.Y., van der M.S., Achtman M., Suerbaum S. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog. 2008, 4:e1000180.
35. Suerbaum S., Maynard Smith J., Bapumia K., Morelli G., Smith N.H., Kunstmann E., Dyrek I., Achtman M. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12619-12624.
36. Suerbaum S., Michetti P. Helicobacter pylori infection. N. Engl. J. Med. 2002, 347:1175-1186.
37. Tatusov R.L., Koonin E.V., Lipman D.J. A genomic perspective on protein families. Science 1997, 278:631-637.
38. Tatusov R.L., Natale D.A., Garkavtsev I.V., Tatusova T.A., Shankavaram U.T., Rao B.S., Kiryutin B., Galperin M.Y., Fedorova N.D., Koonin E.V. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 2001, 29:22-28.
39. Taylor N.S., Fox J.G., Akopyants N.S., Berg D.E., Thompson N., Shames B., Yan L., Fontham E., Janney F., Hunter F.M. Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J. Clin. Microbiol. 1995, 33:918-923.
40. Treangen T.J., Messeguer X. M-GCAT: interactively and efficiently constructing large-scale multiple genome comparison frameworks in closely related species. BMC Bioinform. 2006, 7:433.
41. Yahara K., Kawai M., Furuta Y., Takahashi N., Handa N., Tsuru T., Oshima K., Yoshida M., Azuma T., Hattori M., Uchiyama I., Kobayashi I. Genome-wide survey of mutual homologous recombination in a highly sexual bacterial species. Genome Biol. Evol. 2012, 4:628-640.