Helicobacter pylori evolution and phenotypic diversification in a changing host

Suerbaum, Sebastian; Josenhans, Christine

doi:10.1038/nrmicro1658

Cited by 384Helicobacter pylori-related gastroenterology studiesEvolution and Genetic DynamicsGenetic diversity and population structure

Helicobacter pylori evolution and phenotypic diversification in a changing host

Suerbaum, Sebastian, Josenhans, Christine·2007·Nature Reviews Microbiology

DOI 10.1038/nrmicro1658

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Abstract

Helicobacter pylori colonizes the stomachs of more than 50% of the world's population, making it one of the most successful of all human pathogens. One striking characteristic of H. pylori biology is its remarkable allelic diversity and genetic variability. Not only does almost every infected person harbour their own individual H. pylori strain, but strains can undergo genetic alteration in vivo, driven by an elevated mutation rate and frequent intraspecific recombination. This genetic variability, which affects both housekeeping and virulence genes, has long been thought to contribute to host adaptation, and several recently published studies support this concept. We review the available knowledge relating to the genetic variation of H. pylori, with special emphasis on the changes that occur during chronic colonization, and argue that H. pylori uses mutation and recombination processes to adapt to its individual host by modifying molecules that interact with the host. Finally, we put forward the hypothesis that the lack of opportunity for intraspecies recombination as a result of the decreasing prevalence of H. pylori could accelerate its disappearance from Western populations.

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Bäckström, A., Lundberg, C., Kersulyte, D., Berg, D. E., Borén, T., & Arnqvist, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404817101 · Cited by 143 · see citing works
Phase Variation in Helicobacter pylori Lipopolysaccharide due to Changes in the Lengths of Poly(C) Tracts in α3-Fucosyltransferase Genes
Appelmelk, B. J., Martin, S. L., Monteiro, M. A., Clayton, C. A., McColm, A. A., Zheng, P., Verboom, T., Maaskant, J. J., EIJNDEN, D. H. V. D., Hokke, C. H., et al. (1999) · Infection and Immunity · doi:10.1128/iai.67.10.5361-5366.1999 · Cited by 142 · see citing works
Bacterial populations as perfect gases: genomic integrity and diversification tensions in Helicobacter pylori
Kang, J., & Blaser, M. J. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1528 · Cited by 141 · see citing works
Epidemiology of Helicobacter pylori Infection
Queiroz, D. M. M., & Luzza, F. (2006) · Helicobacter · doi:10.1111/j.1478-405x.2006.00429.x · Cited by 140 · see citing works
Extensive repetitive DNA facilitates prokaryotic genome plasticity
Aras, R. A., Kang, J., Tschumi, A. I., Harasaki, Y., & Blaser, M. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1735481100 · Cited by 138 · see citing works
Genotyping of Helicobacter pylori isolates by sequencing of PCR products and comparison with the RAPD technique
Kansau, I., Raymond, J., Bingen, É., Courcoux, P., Kalach, N., Bergeret, M., Braimi, N., Dupont, C. M., & Labigne-Roussel, A. (1996) · Research in Microbiology · doi:10.1016/0923-2508(96)84023-x · Cited by 137 · see citing works
East Asian genotypes of Helicobacter pylori strains in Amerindians provide evidence for its ancient human carriage
Ghose, C., Perez-Perez, G. I., Domı́nguez-Bello, M.-G., Pride, D. T., Bravi, C. M., & Blaser, M. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242574599 · Cited by 122 · see citing works
Comparison of Genetic Divergence and Fitness between Two Subclones of Helicobacter pylori
Björkholm, B., Lundin, A., Sillén, A., Guillemin, K. J., Salama, N. R., Rubio‐Terres, C., Gordon, J. I., Falk, P. G., & Engstrand, L. G. (2001) · Infection and Immunity · doi:10.1128/iai.69.12.7832-7838.2001 · Cited by 121 · see citing works
Switching of Flagellar Motility in Helicobacter pylori by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in fliP , a Gene Encoding a Basal Body Protein
Josenhans, C., Eaton, K. A., Thevenot, T., & Suerbaum, S. (2000) · Infection and Immunity · doi:10.1128/iai.68.8.4598-4603.2000 · Cited by 105 · see citing works
Self-citation
Helicobacter pylori-host cell interactions mediated by type IV secretion
Bourzac, K. M., & Guillemin, K. J. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00541.x · Cited by 103 · see citing works
The diversity within an expanded and redefined repertoire of phase-variable genes in Helicobacter pylori
Salaün, L., Linz, B., Suerbaum, S., & Saunders, N. J. S. G. (2004) · Microbiology · doi:10.1099/mic.0.26993-0 · Cited by 96 · see citing works
Self-citation
Genetic and Transmission Analysis ofHelicobacter pyloriStrains within a Family1
Raymond, J., Thiberge, J.-M., Chevalier, C., Kalach, N., Bergeret, M., Labigne-Roussel, A., & Dauga, C. (2004) · Emerging infectious diseases · doi:10.3201/eid1010.040042 · Cited by 96 · see citing works
Plasticity of Repetitive DNA Sequences within a Bacterial (Type IV) Secretion System Component
Aras, R. A., Fischer, W. H., Perez-Perez, G. I., Crosatti, M., Ando, T., Haas, R., & Blaser, M. J. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030381 · Cited by 94 · see citing works
Distinct Diversity of the cag Pathogenicity Island among Helicobacter pylori Strains in Japan
Azuma, T., Yamakawa, A., Yamazaki, S., Ohtani, M., Ito, Y., Muramatsu, A., Suto, H., Yamazaki, Y., Keida, Y., Higashi, H., et al. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.6.2508-2517.2004 · Cited by 89 · see citing works
Functional and Intracellular Signaling Differences Associated with the Helicobacter pylori AlpAB Adhesin from Western and East Asian Strains
Lü, H., Wu, J. Y., Beswick, E. J., Ohno, T., Odenbreit, S., Haas, R., Reyes, V. E., Kita, M., Graham, D. Y., & Yamaoka, Y. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611178200 · Cited by 88 · see citing works
ChronicHelicobacter pyloriInfection with Sydney Strain 1 and a Newly Identified Mouse-Adapted Strain (Sydney Strain 2000) in C57BL/6 and BALB/c Mice
Thompson, L. J., Danon, S. J., Wilson, J. E., O’Rourke, J., Salama, N. R., Falkow, S., Mitchell, H. M., & Lee, A. (2004) · Infection and Immunity · doi:10.1128/iai.72.8.4668-4679.2004 · Cited by 87 · see citing works
Genomic Changes during Chronic Helicobacter pylori Infection
Kraft, C., Stack, A., Josenhans, C., Niehus, E., Dietrich, G., Correa, P., Fox, J. G., Falush, D., & Suerbaum, S. (2005) · Journal of Bacteriology · doi:10.1128/jb.188.1.249-254.2006 · Cited by 84 · see citing works
Self-citation
cag A positive and negative Helicobacter pylori strains are simultaneously present in the stomach of most patients with non-ulcer dyspepsia: relevance to histological damage
Figura, N., Vindigni, C., Covacci, A., Presenti, L., Burroni, D., Vernillo, R., Banducci, T., Roviello, F., Marrelli, D., Biscontri, M., et al. (1998) · Gut · doi:10.1136/gut.42.6.772 · Cited by 80 · see citing works
Mutation and recombination in : Mechanisms and role in generating strain diversity
KRAFT, C. (2005) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.06.002 · Cited by 75 · see citing works
Helicobacter pylori: molecular and cellular biology.
Achtman, M., & Suerbaum, S. (2001) · Cited by 75 · see citing works
Self-citation
Helicobacter pylori Mutants Defective in RuvC Holliday Junction Resolvase Display Reduced Macrophage Survival and Spontaneous Clearance from the Murine Gastric Mucosa
Loughlin, M. F., Barnard, F. M., Jenkins, D., Sharples, G. J., & Jenks, P. J. (2003) · Infection and Immunity · doi:10.1128/iai.71.4.2022-2031.2003 · Cited by 73 · see citing works
An enzymatic ruler modulates Lewis antigen glycosylation of Helicobacter pylori LPS during persistent infection
Nilsson, C., Skoglund, A., Moran, A. P., Annuk, H., Engstrand, L. G., & Normark, S. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511119103 · Cited by 70 · see citing works
Helicobacter pylori: molecular evolution of a bacterial quasi-species
Covacci, A., & Rappuoli, R. (1998) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(98)80148-3 · Cited by 66 · see citing works
Characterization of the Pilin Ortholog of theHelicobacter pyloriType IVcagPathogenicity Apparatus, a Surface-Associated Protein Expressed during Infection
Andrzejewska, J., Lee, S. K., Olbermann, P., Lotzing, N., Katzowitsch, E., Linz, B., Achtman, M., Kado, C. I., Suerbaum, S., & Josenhans, C. (2006) · Journal of Bacteriology · doi:10.1128/jb.00060-06 · Cited by 62 · see citing works
Self-citation
Genetic Analysis of Helicobacter pylori Strain Populations Colonizing the Stomach at Different Times Postinfection
Salama, N. R., González-Valencia, G., Deatherage, B. L., Avilés‐Jiménez, F., Atherton, J. C., Graham, D. Y., & Torres, J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01696-06 · Cited by 59 · see citing works
Heterogeneity of Helicobacter pylori cag genotypes in experimentally infected mice
Sozzi, M., Crosatti, M., Kim, S.-K., Romero, J., & Blaser, M. J. (2001) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2001.tb10828.x · Cited by 45 · see citing works
Antimutator Role of the DNA Glycosylase mutY Gene in Helicobacter pylori
Huang, S., Kang, J., & Blaser, M. J. (2006) · Journal of Bacteriology · doi:10.1128/jb.00477-06 · Cited by 45 · see citing works
Microevolution between paired antral and paired antrum and corpus Helicobacter pylori isolates recovered from individual patients
Carroll, I. M., Ahmed, N., Beesley, S. M., Khan, A. A., Ghousunnissa, S., O'Morain, C. A., Habibullah, C., & Smyth, C. J. (2004) · Journal of Medical Microbiology · doi:10.1099/jmm.0.05440-0 · Cited by 42 · see citing works
Pathogen Evolution In Vivo: Genome Dynamics of Two Isolates Obtained 9 Years Apart from a Duodenal Ulcer Patient Infected with a Single Helicobacter pylori Strain
Prouzet‐Mauleon, V., Hussain, M. A., Lamouliatte, H., Kauser, F., Mégraud, F., & Ahmed, N. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.8.4237-4241.2005 · Cited by 39 · see citing works
Slow Genetic Divergence of Helicobacter pylori Strains during Long-Term Colonization
Lundin, A., Björkholm, B., Kupershmidt, I., Unemo, M., Nilsson, P., Andersson, D. I., & Engstrand, L. G. (2005) · Infection and Immunity · doi:10.1128/iai.73.8.4818-4822.2005 · Cited by 39 · see citing works
Host Adaptation and Immune Modulation Are Mediated by Homologous Recombination inHelicobacter pylori
Robinson, K., Loughlin, M. F., Potter, R., & Jenks, P. J. (2005) · The Journal of Infectious Diseases · doi:10.1086/427657 · Cited by 37 · see citing works
Molecular Relationships of Helicobacter Pylori Strains in A Family With Gastroduodenal Disease
Miehlke, S., Genta, R. M., Graham, D. Y., & Go, M. F. (1999) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.1999.859_u.x · Cited by 34 · see citing works
Comparative analysis of the complete cag pathogenicity island sequence in four Helicobacter pylori isolates
Blomstergren, A., Lundin, A., Nilsson, C., Engstrand, L. G., & Lundeberg, J. (2004) · Gene · doi:10.1016/j.gene.2003.11.029 · Cited by 33 · see citing works
Evolution of the Helicobacter pylori Vacuolating Cytotoxin in a Human Stomach
Avilés‐Jiménez, F., Letley, D. P., González-Valencia, G., Salama, N. R., Torres, J., & Atherton, J. C. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.15.5182-5185.2004 · Cited by 30 · see citing works
and the innate immune system
Lee, S. M. L. (2005) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.06.004 · Cited by 19 · see citing works
Helicobacter pylori Genes Involved in Avoidance of Mutations Induced by 8-Oxoguanine
Mathieu, A., O’Rourke, E. J., & Radicella, J. P. (2006) · Journal of Bacteriology · doi:10.1128/jb.00851-06 · Cited by 17 · see citing works
Helicobacter pylori: molecular and cellular biology
Maconi, G. (2002) · Digestive and Liver Disease · doi:10.1016/s1590-8658(02)80100-1 · Cited by 13 · see citing works

Flagged first, then by citations

Sorted by citations

Helicobacter pylori infection
Malfertheiner, P., Camargo, M. C., El-Omar, E. M., Liou, J., Peek, R. M., Schulz, C., Smith, S. I., & Suerbaum, S. (2023) · Nature Reviews Disease Primers · doi:10.1038/s41572-023-00431-8 · Cited by 1,285 · see citing works
Self-citation
Genetic determinants of the gut microbiome in UK twins
Goodrich, J. K., Davenport, E. R., Beaumont, M., Jackson, M. A., Knight, R., Ober, C., Spector, T. D., Bell, J. T., Clark, A. G., & Ley, R. E. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.04.017 · Cited by 1,048 · see citing works
Helicobacter pylori in Health and Disease
Cover, T. L., & Blaser, M. J. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.01.073 · Cited by 716 · see citing works
Within-host evolution of bacterial pathogens
Didelot, X., Walker, A. S., Peto, T., Crook, D. W., & Wilson, D. J. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2015.13 · Cited by 462 · see citing works
ABO Blood Group and the Risk of Pancreatic Cancer
Wolpin, B. M., Chan, A. T., Hartge, P., Chanock, S. J., Kraft, P., Hunter, D. J., Giovannucci, E. L., & Fuchs, C. S. (2009) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djp020 · Cited by 399 · see citing works
Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes
Lieberman, T. D., Michel, J.-B., Aingaran, M., Potter-Bynoe, G., Roux, D., Davis, M. R., Skurnik, D., Leiby, N., LiPuma, J. J., Goldberg, J. B., et al. (2011) · Nature Genetics · doi:10.1038/ng.997 · Cited by 367 · see citing works
Co-occurrence of anaerobic bacteria in colorectal carcinomas
Warren, R. L., Freeman, D. J., Pleasance, S., Watson, P., Moore, R. A., Cochrane, K., Allen-Vercoe, E., & Holt, R. A. (2013) · Microbiome · doi:10.1186/2049-2618-1-16 · Cited by 348 · see citing works
Helicobacter pylori and gastric cancer: mechanisms and new perspectives
Duan, Y., Xu, Y., Dou, Y., & Xu, D. (2025) · Journal of Hematology & Oncology · doi:10.1186/s13045-024-01654-2 · Cited by 311 · see citing works
High-Resolution Transcriptome Maps Reveal Strain-Specific Regulatory Features of Multiple Campylobacter jejuni Isolates
Dugar, G., Herbig, A., Förstner, K. U., Heidrich, N., Reinhardt, R., Nieselt, K., & Sharma, C. M. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003495 · Cited by 275 · see citing works
Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution
Oh, P. L., Benson, A. K., Peterson, D. A., Patil, P. B., Moriyama, E. N., Roos, S., & Walter, J. (2009) · The ISME Journal · doi:10.1038/ismej.2009.123 · Cited by 274 · see citing works
Machine Learning for Antimicrobial Resistance Prediction: Current Practice, Limitations, and Clinical Perspective
Kim, J. I., Maguire, F., Tsang, K. K., Gouliouris, T., Peacock, S. J., McAllister, T. A., McArthur, A. G., & Beiko, R. G. (2022) · Clinical Microbiology Reviews · doi:10.1128/cmr.00179-21 · Cited by 278 · see citing works
Helicobacter pylori adhesin HopQ engages in a virulence-enhancing interaction with human CEACAMs
Javaheri, A., Kruse, T., Moonens, K., Mejías‐Luque, R., Debraekeleer, A., Asche, C. I., Tegtmeyer, N., Kalali, B. N., Bach, N. C., Sieber, S. A., et al. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.189 · Cited by 263 · see citing works
Role of type IV secretion inHelicobacter pyloripathogenesis
Backert, S., & Selbach, M. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01156.x · Cited by 254 · see citing works
Helicobacter pylori genome evolution during human infection
Kennemann, L., Didelot, X., Aebischer, T., Kuhn, S., Drescher, B., Droege, M., Reinhardt, R., Correa, P., Meyer, T. F., Josenhans, C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018444108 · Cited by 249 · see citing works
Self-citation
Evolutionary consequences of drug resistance: shared principles across diverse targets and organisms
Hughes, D., & Andersson, D. I. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3922 · Cited by 243 · see citing works
The 5300-year-old Helicobacter pylori genome of the Iceman
Maixner, F., Krause‐Kyora, B., Turaev, D., Herbig, A., Hoopmann, M. R., Hallows, J. L., Kusebauch, U., Vigl, E. E., Malfertheiner, P., Mégraud, F., et al. (2016) · Science · doi:10.1126/science.aad2545 · Cited by 238 · see citing works
A Global Overview of the Genetic and Functional Diversity in the Helicobacter pylori cag Pathogenicity Island
Olbermann, P., Josenhans, C., Moodley, Y., Uhr, M., Stamer, C., Vauterin, M., Suerbaum, S., Achtman, M., & Linz, B. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001069 · Cited by 235 · see citing works
Self-citation
Helicobacter pylori γ-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance
Oertli, M., Noben, M., Engler, D. B., Semper, R. P., Reuter, S., Maxeiner, J., Gerhard, M., Taube, C., & Mueller, A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211248110 · Cited by 230 · see citing works
The Versatility of Helicobacter pylori CagA Effector Protein Functions: The Master Key Hypothesis
Backert, S., Tegtmeyer, N., & Selbach, M. (2010) · Helicobacter · doi:10.1111/j.1523-5378.2010.00759.x · Cited by 227 · see citing works
Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental Gram-negative bacteria
Seitz, P., & Blokesch, M. (2012) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2012.00353.x · Cited by 222 · see citing works
On the origin of prokaryotic speciesPreprint
Doolittle, W. F., & Zhaxybayeva, O. (2009) · Genome Research · doi:10.1101/gr.086645.108 · Cited by 224 · see citing works
Evolutionary Trajectories to Antibiotic Resistance
Hughes, D., & Andersson, D. I. (2017) · Annual Review of Microbiology · doi:10.1146/annurev-micro-090816-093813 · Cited by 221 · see citing works
Helicobacter pylori Diversity and Gastric Cancer Risk
Cover, T. L. (2016) · mBio · doi:10.1128/mbio.01869-15 · Cited by 217 · see citing works
High Dietary Salt Intake Exacerbates Helicobacter pylori-Induced Gastric Carcinogenesis
Gaddy, J. A., Radin, J. N., Loh, J. T., Zhang, F., Washington, M. K., Peek, R. M., Algood, H. M. S., & Cover, T. L. (2013) · Infection and Immunity · doi:10.1128/iai.01271-12 · Cited by 209 · see citing works
The Role of Helicobacter pylori Outer Membrane Proteins in Adherence and Pathogenesis
Oleastro, M., & Ménard, A. (2013) · Biology · doi:10.3390/biology2031110 · Cited by 183 · see citing works
Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer
Fischer, W. H., Windhager, L., Rohrer, S., Zeiller, M., Karnholz, A., Hoffmann, R. F. G., Zimmer, R., & Haas, R. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq378 · Cited by 180 · see citing works
Horizontal versus Familial Transmission of Helicobacter pylori
Schwarz, S., Morelli, G., Kušećek, B., Manica, A., Balloux, F., Owen, R. J., Graham, D. Y., der Merwe, V., Achtman, M., & Suerbaum, S. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000180 · Cited by 174 · see citing works
Self-citation
Helicobacter pylori-induced gastric pathology: insights from in vivo and ex vivo models
Burkitt, M. D., Duckworth, C. A., Williams, J. M., & Pritchard, D. M. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.027649 · Cited by 178 · see citing works
Survival in hostile territory: the microbiota of the stomach
Yang, I., Nell, S., & Suerbaum, S. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12027 · Cited by 163 · see citing works
Self-citation
Microevolution of Helicobacter pylori during Prolonged Infection of Single Hosts and within Families
Morelli, G., Didelot, X., Kušećek, B., Schwarz, S., Bahlawane, C., Falush, D., Suerbaum, S., & Achtman, M. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001036 · Cited by 152 · see citing works
Self-citation
Within-host evolution of Helicobacter pylori shaped by niche-specific adaptation, intragastric migrations and selective sweeps
Ailloud, F., Didelot, X., Woltemate, S., Pfaffinger, G., Overmann, J., Bader, R., Schulz, C., Malfertheiner, P., & Suerbaum, S. (2019) · Nature Communications · doi:10.1038/s41467-019-10050-1 · Cited by 153 · see citing works
Self-citation
Molecular epidemiology, population genetics, and pathogenic role of Helicobacter pylori
Suzuki, R., Shiota, S., & Yamaoka, Y. (2011) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2011.12.002 · Cited by 151 · see citing works
Genomic evolution and transmission of Helicobacter pylori in two South African families
Didelot, X., Nell, S., Yang, I., Woltemate, S., der Merwe, V., & Suerbaum, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304681110 · Cited by 129 · see citing works
Self-citation
Helicobacter pylori modulates host cell responses by CagT4SS-dependent translocation of an intermediate metabolite of LPS inner core heptose biosynthesis
Stein, S. C., Faber, E., Bats, S. H., Murillo, T., Speidel, Y., Coombs, N., & Josenhans, C. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006514 · Cited by 131 · see citing works
Self-citation
The complex methylome of the human gastric pathogen Helicobacter pylori
Krebes, J., Morgan, R., Bunk, B., Spröer, C., Luong, K., Parusel, R., Anton, B. P., König, C., Josenhans, C., Overmann, J., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1201 · Cited by 121 · see citing works
Self-citation
Parasite Susceptibility to Amphotericin B in Failures of Treatment for Visceral Leishmaniasis in Patients Coinfected with HIV Type 1 andLeishmania infantum
Lachaud, L., Bourgeois, N., Plourde, M., Leprohon, P., Bastien, P., & Ouellette, M. (2008) · Clinical Infectious Diseases · doi:10.1086/595710 · Cited by 118 · see citing works
The Human Gastric PathogenHelicobacter pyloriand Its Association with Gastric Cancer and Ulcer Disease
Bauer, B., & Meyer, T. F. (2011) · Ulcers · doi:10.1155/2011/340157 · Cited by 113 · see citing works
Structural Insights into Polymorphic ABO Glycan Binding by Helicobacter pylori
Moonens, K., Gideonsson, P., Subedi, S., Bugaytsova, J. A., Romão, E., Méndez, M., Nordén, J., Fallah, M., Rakhimova, L., Shevtsova, A. A., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2015.12.004 · Cited by 113 · see citing works
Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer
McClain, M. S., Shaffer, C. L., Israel, D. A., Peek, R. M., & Cover, T. L. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-3 · Cited by 113 · see citing works
Strategies used by helicobacter pylori to establish persistent infection
Abadi, A. T. B. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i16.2870 · Cited by 114 · see citing works
Outer Membrane Protein Expression Profile in Helicobacter pylori Clinical Isolates
Odenbreit, S., Swoboda, K., Barwig, I., Rühl, S., Borén, T., Koletzko, S., & Haas, R. (2009) · Infection and Immunity · doi:10.1128/iai.00364-09 · Cited by 111 · see citing works
Genetic Diversity in the Oral Pathogen Porphyromonas Gingivalis : Molecular Mechanisms and Biological Consequences
Tribble, G. D., Kerr, J., & Wang, B.-Y. (2013) · Future Microbiology · doi:10.2217/fmb.13.30 · Cited by 110 · see citing works
Helicobacter pylori treatment in the post-antibiotics era—searching for new drug targets
Roszczenko, P., Wojtyś, M. I., & Jagusztyn-Krynicka, E. K. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-10945-w · Cited by 110 · see citing works
Helicobacter pylori gene silencing in vivo demonstrates urease is essential for chronic infection
Debowski, A. W., Walton, S. M., Chua, E. G., Tay, C. Y., Liao, T., Lamichhane, B., Himbeck, R. P., Stubbs, K. A., Marshall, B. J., Fulurija, A., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006464 · Cited by 105 · see citing works
Common Coinfections of Giardia intestinalis and Helicobacter pylori in Non-Symptomatic Ugandan Children
Ankarklev, J., Hestvik, E., Lebbad, M., Lindh, J. G., Kaddu-Mulindwa, D. H., Andersson, J. O., Tylleskär, T., Tumwine, J. K., & Svärd, S. G. (2012) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001780 · Cited by 105 · see citing works
Helicobacter pylori typing as a tool for tracking human migration
Yamaoka, Y. (2009) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2009.02967.x · Cited by 101 · see citing works
NATURAL TRANSFORMATION INCREASES THE RATE OF ADAPTATION IN THE HUMAN PATHOGEN HELICOBACTER PYLORI
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Authors: Suerbaum, S., & Josenhans, C.
Affiliations: Medizinische Hochschule Hannover (DE)
ORCID: Suerbaum, Sebastian
Josenhans, Christine
Venue: Nature Reviews Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2007-06
Volume: 5
Issue: 6
Pages: 441-452
ISSN: 1740-1526 (ISSN-L)
1740-1534
DOI: 10.1038/nrmicro1658
OpenAlex: W2015449706
Cited by: 384
References: 112
Citations by year: 2026: 13 · 2025: 13 · 2024: 14 · 2023: 13 · 2022: 12 · 2021: 17 · 2020: 14 · 2019: 26 · 2018: 18 · 2017: 28 · 2016: 31 · 2015: 10 · 2014: 23 · 2013: 27 · 2012: 27
FWCI: 4.38
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Microbiology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Keywords: Helicobacter pylori, genetic diversity, host adaptation, phenotypic diversification, mutation rate, virulence genes, chronic colonization, host-pathogen interaction, declining prevalence, Western populations
MeSH terms: Adaptation, Biological, Biological Evolution, Humans, Mutation, Recombination, Genetic, Stomach Neoplasms, Genetic Variation, Helicobacter pylori

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Helicobacter pylori evolution and phenotypic diversification in a changing host

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