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A variable gene in a conserved region of the Helicobacter pylori genome: isotopic gene replacement or rapid evolution?

ABSTRACT: The present study concerns the identification of a novel coding sequence in a region of the Helicobacter pylori genome, located between JHP1069/HP1141 and JHP1071/HP1143 according to the numbering of the J99 and 26,695 reference strains, respectively, and spanning three different coding DNA sequences (CDSs). The CDSs located at the centre of this locus were highly polymorphic, as determined by the analysis of 24 European isolates, 3 Asian, and 3 African isolates. Phylogenetic and molecular evolutionary analyses showed that the CDSs were not restricted to the geographical origin of the strains. Despite a very high variability observed in the deduced protein sequences, significant similarity was observed, always with the same protein families, i.e. ATPase and bacteriophage receptor/invasion proteins. Although this variability could be explained by isotopic gene replacement via horizontal transfer of a gene with the same function but coming from a variety of sources, it seems more likely that the very high sequence variation observed at this locus is the result of a strong selection pressure exerted on the corresponding gene product. The CDSs identified in the present study could be used as strain specific markers.

SUBMITTER: Menard A

PROVIDER: S-EPMC2650637 | biostudies-literature | 2008 Jun

REPOSITORIES: biostudies-literature

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A variable gene in a conserved region of the Helicobacter pylori genome: isotopic gene replacement or rapid evolution?

Ménard Armelle A Danchin Antoine A Dupouy Sandrine S Mégraud Francis F Lehours Philippe P

DNA research : an international journal for rapid publication of reports on genes and genomes 20080427 3

The present study concerns the identification of a novel coding sequence in a region of the Helicobacter pylori genome, located between JHP1069/HP1141 and JHP1071/HP1143 according to the numbering of the J99 and 26,695 reference strains, respectively, and spanning three different coding DNA sequences (CDSs). The CDSs located at the centre of this locus were highly polymorphic, as determined by the analysis of 24 European isolates, 3 Asian, and 3 African isolates. Phylogenetic and molecular evolu ...[more]

PMID: 18442984

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Project description:BackgroundThe cytotoxin-associated gene A (cagA) is one of the most important virulence factors of Helicobacter pylori (H. pylori). There is a highly polymorphic Glu-Pro-Ile-Tyr-Ala (EPIYA) repeat region in the C-terminal of CagA protein. This repeat region is thought to play an important role in the pathogenesis of gastrointestinal diseases. The aim of this study was to investigate the diversity of cagA 3' variable region and the amino acid polymorphisms in the EPIYA segments of the CagA C-terminal region of H. pylori, and their association with gastroduodenal diseases.MethodsA total of 515 H. pylori strains from patients in 14 different geographical regions of China were collected. The genomic DNA from each strain was extracted and the cagA 3' variable region was amplified by polymerase chain reaction (PCR). The PCR products were sequenced and analyzed using MEGA 7.0 software.ResultsA total of 503 (97.7%) H. pylori strains were cagA-positive and 1,587 EPIYA motifs were identified, including 12 types of EPIYA or EPIYA-like sequences. In addition to the four reported major segments, several rare segments (e.g., B', B″ and D') were defined and 20 different sequence types (e.g., ABD, ABC) were found in our study. A total of 481 (95.6%) strains carried the East Asian type CagA, and the ABD subtypes were most prevalent (82.1%). Only 22 strains carried the Western type CagA, which included AC, ABC, ABCC and ABCCCC subtypes. The CagA-ABD subtype had statistical difference in different geographical regions (P = 0.006). There were seven amino acid polymorphisms in the sequences surrounding the EPIYA motifs, among which amino acids 893 and 894 had a statistical difference with gastric cancer (P = 0.004).ConclusionsIn this study, 503 CagA sequences were studied and analyzed in depth. In Chinese population, most H. pylori strains were of the CagA-ABD subtype and its presence was associated with gastroduodenal diseases. Amino acid polymorphisms at residues 893 and 894 flanking the EPIYA motifs had a statistically significant association with gastric cancer.

Project description:BackgroundHelicobacter pylori is a human stomach pathogen, naturally-competent for DNA uptake, and prone to homologous recombination. Extensive homoplasy (i.e., phylogenetically-unlinked identical variations) observed in H. pylori genes is considered a hallmark of such recombination. However, H. pylori also exhibits a high mutation rate. The relative adaptive role of homologous recombination and mutation in species diversity is a highly-debated issue in biology. Recombination results in homoplasy. While convergent mutation can also account for homoplasy, its contribution is thought to be minor. We demonstrate here that, contrary to dogma, convergent mutation is a key contributor to Helicobacter pylori homoplasy, potentially driven by adaptive evolution of proteins.ResultsOur present genome-wide analysis shows that homoplastic nonsynonymous (amino acid replacement) changes are not typically accompanied by homoplastic synonymous (silent) variations. Moreover, the majority of the codon positions with homoplastic nonsynonymous changes also contain different (i.e. non-homoplastic) nonsynonymous changes arising from mutation only. This indicates that, to a considerable extent, nonsynonymous homoplasy is due to convergent mutations. High mutation rate or limited availability of evolvable sites cannot explain this excessive convergence, as suggested by our simulation studies. Rather, the genes with convergent mutations are overrepresented in distinct functional categories, suggesting possible selective responses to conditions such as distinct micro-niches in single hosts, and to differences in host genotype, physiology, habitat and diet.ConclusionsWe propose that mutational convergence is a key player in H. pylori's adaptation and extraordinary persistence in human hosts. High frequency of mutational convergence could be due to saturation of evolvable sites capable of responding to selection pressures, while the number of mutable residues is far from saturation. We anticipate a similar scenario of mutational vs. recombinational genome dynamics or plasticity for other naturally competent microbes where strong positive selection could favor frequent convergent mutations in adaptive protein evolution.

Dataset Information

A variable gene in a conserved region of the Helicobacter pylori genome: isotopic gene replacement or rapid evolution?

Publications

A variable gene in a conserved region of the Helicobacter pylori genome: isotopic gene replacement or rapid evolution?

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