Abstract
Helicobacter pylori infects more than half of the world’s population, making it the most widespread infection of bacteria. It has high genetic diversity and has been considered as one of the most variable bacterial species. In the present study, a PCR-based method was used to detect the presence and the relative frequency of homologous recombination between repeat sequences (>500 bp) in H. pylori 26695. All the recombinant structures have been confirmed by sequencing. The inversion generated between inverted repeats showed distinct features from the recombination for duplication or deletion between direct repeats. Meanwhile, we gave the mathematic reasoning of a general formula for the calculation of relative recombination frequency and indicated the conditions for its application. This formula could be extensively applied to detect the frequency of homologous recombination, site-specific recombination, and other types of predictable recombination. Our results should be helpful for better understanding the genome evolution and adaptation of bacteria.
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References
Graham DY (2000) Therapy of Helicobacter pylori: current status and issues. Gastroenterology 118(2 Suppl 1):S2–S8
Warren J, Robin BM (1983) Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1:1273–1275
Peek RM Jr, Blaser MJ (2002) Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2:28–37
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
Bjorkholm B, Sjolund M, Falk PG, Berg OG, Engstrand L, Andersson DI (2001) Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci USA 98:14607–14612
Lara-Ramirez EE, Segura-Cabrera A, Guo X, Yu G, Garcia-Perez CA, Rodriguez-Perez MA (2011) New implications on genomic adaptation derived from the Helicobacter pylori genome comparison. PLoS One 6(2):e17300. doi:10.1371/journal.pone.0017300
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
Kersulyte D, Kalia A, Zhang M, Lee HK, Subramaniam D, Kiuduliene L, Chalkauskas H, Berg DE (2004) Sequence organization and insertion specificity of the novel chimeric ISHp609 transposable element of Helicobacter pylori. J Bacteriol 186:7521–7528
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(18):6089–6101. doi:10.1093/nar/gkq378
Kersulyte D, Kalia A, Gilman RH, Mendez M, Herrera P, Cabrera L, Velapatino B, Balqui J, Puente Paredes, de la Vega F, Rodriguez Ulloa CA, Cok J, Hooper CC, Dailide G, Tamma S, Berg DE (2010) Helicobacter pylori from Peruvian amerindians: traces of human migrations in strains from remote Amazon, and genome sequence of an Amerind strain. PLoS One 5(11):e15076. doi:10.1371/journal.pone.0015076
Kraft C, Suerbaum S (2005) Mutation and recombination in Helicobacter pylori: mechanisms and role in generating strain diversity. Int J Med Microbiol 295:299–305
Falush D, Kraft C, Taylor NS, Correa P, Fox JG, Achtman M, Suerbaum S (2001) Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci USA 98:15056–15061
Rocha EP, Cornet E, Michel B (2005) Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet 1(2):e15. doi:10.1371/journal.pgen.0010015
Honma M, Zhang LS, Hayashi M, Takeshita K, Nakagawa Y, Tanaka N, Sofuni T (1997) Illegitimate recombination leading to allelic loss and unbalanced translocation in p53-mutated human lymphoblastoid cells. Mol Cell Biol 17:4774–4781
Segall A, Mahan MJ, Roth JR (1988) Rearrangement of the bacterial chromosome: forbidden inversions. Science 241:1314–1318
Bi X, Liu LF (1996) DNA rearrangement mediated by inverted repeats. Proc Natl Acad Sci USA 93:819–823
Furuta Y, Kawai M, Yahara K, Takahashi N, Handa N, Tsuru T, Oshima K, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I (2011) Birth and death of genes linked to chromosomal inversion. Proc Natl Acad Sci USA 108:1501–1506
Tillier ER, Collins RA (2000) Genome rearrangement by replication-directed translocation. Nat Genet 26:195–197
Chedin F, Dervyn E, Dervyn R, Ehrlich SD, Noirot P (1994) Frequency of deletion formation decreases exponentially with distance between short direct repeats. Mol Microbiol 12:561–569
Aras RA, Kang J, Tschumi AI, Harasaki Y, Blaser MJ (2003) Extensive repetitive DNA facilitates prokaryotic genome plasticity. Proc Natl Acad Sci USA 100:13579–13584
Dworkin J, Blaser MJ (1997) Nested DNA inversion as a paradigm of programmed gene rearrangement. Proc Natl Acad Sci USA 94:985–990
Antonio-Rincon F, Lopez-Vidal Y, Castillo-Rojas G, Lazcano-Ponce EC, Ponce-de-Leon S, Tabche-Barrera ML, Aguilar-Gutierrez GR (2011) Pathogenicity island cag, vacA and IS605 genotypes in Mexican strains of Helicobacter pylori associated with peptic ulcers. Ann Clin Microbiol Antimicrob 10:18. doi:10.1186/1476-0711-10-18
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642
Guo X, Flores M, Mavingui P, Fuentes SI, Hernandez G, Davila G, Palacios R (2003) Natural genomic design in Sinorhizobium meliloti: novel genomic architectures. Genome Res 13(8):1810–1817. doi:10.1101/gr.1260903
Mavingui P, Flores M, Guo X, Davila G, Perret X, Broughton WJ, Palacios R (2002) Dynamics of genome architecture in Rhizobium sp. strain NGR234. J Bacteriol 184:171–176
Flores M, Mavingui P, Perret X, Broughton WJ, Romero D, Hernandez G, Davila G, Palacios R (2000) Prediction, identification, and artificial selection of DNA rearrangements in Rhizobium: toward a natural genomic design. Proc Natl Acad Sci USA 97:9138–9143
Dorer MS, Sessler TH, Salama NR (2011) Recombination and DNA repair in Helicobacter pylori. Annu Rev Microbiol 65:329–348
Suerbaum S, Smith JM, Bapumia K, Morelli G, Smith NH, Kunstmann E, Dyrek I, Achtman M (1998) Free recombination within Helicobacter pylori. Proc Natl Acad Sci USA 95:12619–12624
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 USA 108(12):5033–5038. doi:10.1073/pnas.1018444108
Morelli G, Didelot X, Kusecek B, Schwarz S, Bahlawane C, Falush D, Suerbaum S, Achtman M (2010) Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 6(7):e1001036. doi:10.1371/journal.pgen.1001036
Acknowledgments
The authors are very grateful to Dr. Nina R. Salama for her kind help in providing them some genomic DNA of Helicobacter pylori. Xianwu Guo and Mario A. Rodríguez-Pérez hold a scholarship from Comisión de Operación y Fomento de Actividades Académicas/Instituto Politécnico Nacional. This work was supported by the Consejo Nacional de Ciencia y Tecnología-México (http://www.conacyt.gob.mx/convocatorias/Paginas/default.aspx) (Fondo Sectorial de Investigación Básica SEP CONACyT (CB-2011-01) with Grant number: 168541); and Secretaría de Investigación y Posgrado del Instituto Politécnico Nacional, México (http://www.sip.ipn.mx/WPS/WCM/CONNECT/SIP/SIP/INICIO/INDEX.HTM) (Grant numbers: SIP20120202).
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Yajuan Fu and Reyna Cristina Zepeda-Gurrola have contributed equally to this study.
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Fu, Y., Zepeda-Gurrola, R.C., Aguilar-Gutiérrez, G.R. et al. The Detection of Inherent Homologous Recombination Between Repeat Sequences in H. pylori 26695 by the PCR-Based Method. Curr Microbiol 68, 211–219 (2014). https://doi.org/10.1007/s00284-013-0466-7
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DOI: https://doi.org/10.1007/s00284-013-0466-7