期刊论文详细信息
BMC Microbiology
Phylogeographic evidence of cognate recognition site patterns and transformation efficiency differences in H. pylori: theory of strain dominance
María Gloria Domínguez-Bello4  Martin J Blaser6  Bodo Linz2  Monica Contreras5  Teresa Alarcón1  Luis Pericchi7  Xue-Song Zhang4  Shrinivasrao P Mane3  Ana Maldonado-Contreras8 
[1] Servicio de Microbiología, Hospital Universitario de la Princesa, Madrid, Spain;Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA, USA;Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, VA, USA;Department of Medicine, New York University Langone Medical Center, Manhattan, NY, USA;Venezuelan Institute of Scientific Research (IVIC), San Antonio de los Altos, Venezuela;New York Harbor Veterans Affairs Medical Center, Manhattan, NY, USA;Department of Mathematic, University of Puerto Rico, Río Piedras, San Juan, USA;Microbiology and Physiological Systems Department, University of Massachusetts Medical School, Worcester, MA, USA
关键词: Recombination;    Restriction-Modification system;    Haplotypes;    H. pylori;   
Others  :  1143049
DOI  :  10.1186/1471-2180-13-211
 received in 2013-02-20, accepted in 2013-08-28,  发布年份 2013
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【 摘 要 】

Background

Helicobacter pylori has diverged in parallel to its human host, leading to distinct phylogeographic populations. Recent evidence suggests that in the current human mixing in Latin America, European H. pylori (hpEurope) are increasingly dominant at the expense of Amerindian haplotypes (hspAmerind). This phenomenon might occur via DNA recombination, modulated by restriction-modification systems (RMS), in which differences in cognate recognition sites (CRS) and in active methylases will determine direction and frequency of gene flow. We hypothesized that genomes from hspAmerind strains that evolved from a small founder population have lost CRS for RMS and active methylases, promoting hpEurope’s DNA invasion. We determined the observed and expected frequencies of CRS for RMS in DNA from 7 H. pylori whole genomes and 110 multilocus sequences. We also measured the number of active methylases by resistance to in vitro digestion by 16 restriction enzymes of genomic DNA from 9 hpEurope and 9 hspAmerind strains, and determined the direction of DNA uptake in co-culture experiments of hspAmerind and hpEurope strains.

Results

Most of the CRS were underrepresented with consistency between whole genomes and multilocus sequences. Although neither the frequency of CRS nor the number of active methylases differ among the bacterial populations (average 8.6 ± 2.6), hspAmerind strains had a restriction profile distinct from that in hpEurope strains, with 15 recognition sites accounting for the differences. Amerindians strains also exhibited higher transformation rates than European strains, and were more susceptible to be subverted by larger DNA hpEurope-fragments than vice versa.

Conclusions

The geographical variation in the pattern of CRS provides evidence for ancestral differences in RMS representation and function, and the transformation findings support the hypothesis of Europeanization of the Amerindian strains in Latin America via DNA recombination.

【 授权许可】

   
2013 Maldonado-Contreras et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H, Schlebusch CM, Bernhoft S, Hale J, Suerbaum S, Mugisha L, et al.: Age of the association between Helicobacter pylori and man. PLoS Pathog 2012, 8(5):e1002693.
  • [2]Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, et al.: An African origin for the intimate association between humans and Helicobacter pylori. Nature 2007, 445(7130):915-918.
  • [3]Nobusato A, Uchiyama I, Kobayashi I: Diversity of restriction-modification gene homologues in Helicobacter pylori. Gene 2000, 259(1–2):89-98.
  • [4]Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, et al.: Traces of human migrations in Helicobacter pylori populations. Science 2003, 299(5612):1582-1585.
  • [5]Baltrus DA, Guillemin K, Phillips PC: Natural transformation increases the rate of adaptation in the human pathogen Helicobacter pylori. Evolution 2008, 62(1):39-49.
  • [6]van Doorn LJ, Figueiredo C, Sanna R, Pena S, Midolo P, Ng EK, Atherton JC, Blaser MJ, Quint WG: Expanding allelic diversity of Helicobacter pylori vacA. J Clin Microbiol 1998, 36(9):2597-2603.
  • [7]Kersulyte D, Mukhopadhyay AK, Velapatino B, Su W, Pan Z, Garcia C, Hernandez V, Valdez Y, Mistry RS, Gilman RH, et al.: Differences in genotypes of Helicobacter pylori from different human populations. J Bacteriol 2000, 182(11):3210-3218.
  • [8]Owen RJ, Xerry J: Geographical conservation of short inserts in the signal and middle regions of the Helicobacter pylori vacuolating cytotoxin gene. Microbiology 2007, 153(Pt 4):1176-1186.
  • [9]Ghose C, Perez-Perez GI, van Doorn LJ, Dominguez-Bello MG, Blaser MJ: High frequency of gastric colonization with multiple Helicobacter pylori strains in Venezuelan subjects. J Clin Microbiol 2005, 43(6):2635-2641.
  • [10]Dominguez-Bello MG, Perez ME, Bortolini MC, Salzano FM, Pericchi LR, Zambrano-Guzman O, Linz B: Amerindian Helicobacter pylori strains go extinct, as european strains expand their host range. PLoS ONE 2008, 3(10):e3307.
  • [11]Suerbaum S, Smith JM, Bapumia K, Morelli G, Smith NH, Kunstmann E, Dyrek I, Achtman M: Free recombination within Helicobacter pylori. Proc Natl Acad Sci U S A 1998, 95(21):12619-12624.
  • [12]Kuipers EJ, Israel DA, Kusters JG, Blaser MJ: Evidence for a conjugation-like mechanism of DNA transfer in Helicobacter pylori. J Bacteriol 1998, 180(11):2901-2905.
  • [13]Suerbaum S, Achtman M: Evolution of Helicobacter pylori: the role of recombination. Trends Microbiol 1999, 7(5):182-184.
  • [14]Israel DA, Salama N, Krishna U, Rieger UM, Atherton JC, Falkow S, Peek RM Jr: Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc Natl Acad Sci USA 2001, 98(25):14625-14630.
  • [15]Kuipers EJ, Israel DA, Kusters JG, Gerrits MM, Weel J, van Der Ende A, van Der Hulst RW, Wirth HP, Hook-Nikanne J, Thompson SA, et al.: Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. J Infect Dis 2000, 181(1):273-282.
  • [16]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(7):e1001036.
  • [17]Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, Droege M, Reinhardt R, Correa P, Meyer TF, Josenhans C, et al.: Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci USA 2011, 108(12):5033-5038.
  • [18]Aras RA, Small AJ, Ando T, Blaser MJ: Helicobacter pylori interstrain restriction-modification diversity prevents genome subversion by chromosomal DNA from competing strains. Nucleic Acids Res 2002, 30(24):5391-5397.
  • [19]Achtman M, Azuma T, Berg DE, Ito Y, Morelli G, Pan ZJ, Suerbaum S, Thompson SA, van der Ende A, van Doorn LJ: Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol 1999, 32(3):459-470.
  • [20]Suerbaum S, Achtman M: Helicobacter pylori: recombination, population structure and human migrations. Int J Med Microbiol 2004, 294(2–3):133-139.
  • [21]Furuta Y, Yahara K, Hatakeyama M, Kobayashi I: Evolution of cagA oncogene of Helicobacter pylori through recombination. PLoS ONE 2011, 6(8):e23499.
  • [22]Arber W: Host-controlled modification of bacteriophage. Annu Rev Microbiol 1965, 19:365-378.
  • [23]Kobayashi I: Restriction-Modification systems as a minimal forms of life from restriction endonucleases. Vol. 14: Gross HJ. Berlin, Heidelberg: Springer-Verlag; 2004.
  • [24]Lin LF, Posfai J, Roberts RJ, Kong H: Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc Natl Acad Sci U S A 2001, 98(5):2740-2745.
  • [25]Xu Q, Morgan RD, Roberts RJ, Blaser MJ: Identification of type II restriction and modification systems in Helicobacter pylori reveals their substantial diversity among strains. Proc Natl Acad Sci U S A 2000, 97(17):9671-9676.
  • [26]Wilson GG, Murray NE: Restriction and modification systems. Annu Rev Genet 1991, 25:585-627.
  • [27]Kobayashi I: Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res 2001, 29(18):3742-3756.
  • [28]Rocha EP, Danchin A, Viari A: Evolutionary role of restriction/modification systems as revealed by comparative genome analysis. Genome Res 2001, 11(6):946-958.
  • [29]Panina EM, Mironov AA, Gel’fand MS: Statistical analysis of complete bacterial genomes: palindromes and systems of restriction-modification. Mol Biol (Mosk) 2000, 34(2):246-252.
  • [30]Gelfand MS, Koonin EV: Avoidance of palindromic words in bacterial and archaeal genomes: a close connection with restriction enzymes. Nucleic Acids Res 1997, 25(12):2430-2439.
  • [31]Levine SM, Lin EA, Emara W, Kang J, DiBenedetto M, Ando T, Falush D, Blaser MJ: Plastic cells and populations: DNA substrate characteristics in Helicobacter pylori transformation define a flexible but conservative system for genomic variation. Faseb J 2007, 21(13):3458-3467.
  • [32]Zhang XS, Blaser MJ: Natural transformation of an engineered Helicobacter pylori strain deficient in type II restriction endonucleases. J Bacteriol 2012, 194(13):3407-3416.
  • [33]Pride DT, Blaser M: Identification of horizontally acquired genetic elements in Helicobacter pylori and other prokaryotes using oligonucleotide difference analysis. Genome Letters 2002, 1(1):2-15.
  • [34]Schroeder C, Jurkschat H, Meisel A, Reich JG, Kruger D: Unusual occurrence of EcoP1 and EcoP15 recognition sites and counter-selection of type II methylation and restriction sequences in bacteriophage T7 DNA. Gene 1986, 45(1):77-86.
  • [35]Boyer HW: DNA restriction and modification mechanisms in bacteria. Annu Rev Microbiol 1971, 25:153-176.
  • [36]Revel HR, Luria SE: DNA-glucosylation in T-even phage: genetic determination and role in phage-host interaction. Annu Rev Genet 1970, 4:177-192.
  • [37]Price C, Bickle TA: A possible role for DNA restriction in bacterial evolution. Microbiol Sci 1986, 3(10):296-299.
  • [38]Karlin S, Burge C, Campbell AM: Statistical analyses of counts and distributions of restriction sites in DNA sequences. Nucleic Acids Res 1992, 20(6):1363-1370.
  • [39]Burge C, Campbell AM, Karlin S: Over- and under-representation of short oligonucleotides in DNA sequences. Proc Natl Acad Sci USA 1992, 89(4):1358-1362.
  • [40]Wang MX, Church GM: A whole genome approach to in vivo DNA-protein interactions in E. coli. Nature 1992, 360(6404):606-610.
  • [41]Campbell JL, Kleckner N: E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 1990, 62(5):967-979.
  • [42]Takata T, Aras R, Tavakoli D, Ando T, Olivares AZ, Blaser MJ: Phenotypic and genotypic variation in methylases involved in type II restriction-modification systems in Helicobacter pylori. Nucleic Acids Res 2002, 30(11):2444-2452.
  • [43]Vale FF, Vitor JM: Genomic methylation: a tool for typing Helicobacter pylori isolates. Appl Environ Microbiol 2007, 73(13):4243-4249.
  • [44]Ando T, Ishiguro K, Watanabe O, Miyake N, Kato T, Hibi S, Mimura S, Nakamura M, Miyahara R, Ohmiya N, et al.: Restriction-modification systems may be associated with Helicobacter pylori virulence. J Gastroenterol Hepatol 2010, 25(Suppl 1):S95-S98.
  • [45]Naito T, Kusano K, Kobayashi I: Selfish behavior of restriction-modification systems. Science 1995, 267(5199):897-899.
  • [46]Handa N, Kobayashi I: Post-segregational killing by restriction modification gene complexes: observations of individual cell deaths. Biochimie 1999, 81(8–9):931-938.
  • [47]Donahue JP, Israel DA, Torres VJ, Necheva AS, Miller GG: Inactivation of a Helicobacter pylori DNA methyltransferase alters dnaK operon expression following host-cell adherence. FEMS Microbiol Lett 2002, 208(2):295-301.
  • [48]Takeuchi H, Israel DA, Miller GG, Donahue JP, Krishna U, Gaus K, Peek RM Jr: Characterization of expression of a functionally conserved Helicobacter pylori methyltransferase-encoding gene within inflamed mucosa and during in vitro growth. J Infect Dis 2002, 186(8):1186-1189.
  • [49]Bauman R: Microbiology. San Francisco, CA: Benjamin-Cummings Publishing Company; 2004.
  • [50]Lorenz MG, Wackernagel W: Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 1994, 58(3):563-602.
  • [51]Kang J, Blaser MJ: Bacterial populations as perfect gases: genomic integrity and diversification tensions in Helicobacter pylori. Nat Rev Microbiol 2006, 4(11):826-836.
  • [52]Hofreuter D, Odenbreit S, Henke G, Haas R: Natural competence for DNA transformation in Helicobacter pylori: identification and genetic characterization of the comB locus. Mol Microbiol 1998, 28(5):1027-1038.
  • [53]Smeets LC, Kusters JG: Natural transformation in Helicobacter pylori: DNA transport in an unexpected way. Trends Microbiol 2002, 10(4):159-162. Response from Dirk Hofreuter and Rainer Haas, discussion 162
  • [54]Chang KC, Yeh YC, Lin TL, Wang JT: Identification of genes associated with natural competence in Helicobacter pylori by transposon shuttle random mutagenesis. Biochem Biophys Res Commun 2001, 288(4):961-968.
  • [55]Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, Roche N, Vikstrom S, Sjostrom R, Linden S, Backstrom A, et al.: Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004, 305(5683):519-522.
  • [56]Ando T, Israel DA, Kusugami K, Blaser MJ: HP0333, a member of the dprA family, is involved in natural transformation in Helicobacter pylori. J Bacteriol 1999, 181(18):5572-5580.
  • [57]Smeets LC, Bijlsma JJ, Kuipers EJ, Vandenbroucke-Grauls CM, Kusters JG: The dprA gene is required for natural transformation of Helicobacter pylori. FEMS Immunol Med Microbiol 2000, 27(2):99-102.
  • [58]Jolley KA, Chan MS, Maiden MC: mlstdbNet - distributed multi-locus sequence typing (MLST) databases. BMC Bioinforma 2004, 5:86. BioMed Central Full Text
  • [59]Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, et al.: Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 1998, 95(6):3140-3145.
  • [60]Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 2003, 164(4):1567-1587.
  • [61]Tamura K, Nei M, Kumar S: Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 2004, 101(30):11030-11035.
  • [62]Tamura K, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 2011, 28(10):2731-2739.
  • [63]Kong H, Lin LF, Porter N, Stickel S, Byrd D, Posfai J, Roberts RJ: Functional analysis of putative restriction-modification system genes in the Helicobacter pylori J99 genome. Nucleic Acids Res 2000, 28(17):3216-3223.
  • [64]McCune A, Grace JB, Urban DL: Analysis of ecological communities. Oregon: MJM Software Design; 2001.
  • [65]Clarke KR: Non-parametric multivariate analyses of changes in community structure. Austral Ecol 1993, 18(1):117-143.
  • [66]Buck GE, Smith JS: Medium supplementation for growth of Campylobacter pyloridis. J Clin Microbiol 1987, 25(4):597-599.
  • [67]Miles AA, Misra SS, Irwin JO: The estimation of the bactericidal power of the blood. J Hyg (Lond) 1938, 38(6):732-749.
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