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Role of energy sensor TlpD of Helicobacter pylori in gerbil colonization and genome analyses after adaptation in the gerbil.

ABSTRACT: Helicobacter pylori maintains colonization in its human host using a limited set of taxis sensors. TlpD is a proposed energy taxis sensor of H. pylori and dominant under environmental conditions of low bacterial energy yield. We studied the impact of H. pylori TlpD on colonization in vivo using a gerbil infection model which closely mimics the gastric physiology of humans. A gerbil-adapted H. pylori strain, HP87 P7, showed energy-dependent behavior, while its isogenic tlpD mutant lost it. A TlpD-complemented strain regained the wild-type phenotype. Infection of gerbils with the complemented strain demonstrated that TlpD is important for persistent infection in the antrum and corpus and suggested a role of TlpD in horizontal navigation and persistent corpus colonization. As a part of the full characterization of the model and to gain insight into the genetic basis of H. pylori adaptation to the gerbil, we determined the complete genome sequences of the gerbil-adapted strain HP87 P7, two HP87 P7 tlpD mutants before and after gerbil passage, and the original human isolate, HP87. The integrity of the genome, including that of a functional cag pathogenicity island, was maintained after gerbil adaptation. Genetic and phenotypic differences between the strains were observed. Major differences between the gerbil-adapted strain and the human isolate emerged, including evidence of recent recombination. Passage of the tlpD mutant through the gerbil selected for gain-of-function variation in a fucosyltransferase gene, futC (HP0093). In conclusion, a gerbil-adapted H. pylori strain with a stable genome has helped to establish that TlpD has important functions for persistent colonization in the stomach.

SUBMITTER: Behrens W

PROVIDER: S-EPMC3811781 | biostudies-literature | 2013 Oct

REPOSITORIES: biostudies-literature

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Role of energy sensor TlpD of Helicobacter pylori in gerbil colonization and genome analyses after adaptation in the gerbil.

Behrens Wiebke W Schweinitzer Tobias T Bal Joena J Dorsch Martina M Bleich André A Kops Friederike F Brenneke Birgit B Didelot Xavier X Suerbaum Sebastian S Josenhans Christine C

Infection and immunity 20130708 10

Helicobacter pylori maintains colonization in its human host using a limited set of taxis sensors. TlpD is a proposed energy taxis sensor of H. pylori and dominant under environmental conditions of low bacterial energy yield. We studied the impact of H. pylori TlpD on colonization in vivo using a gerbil infection model which closely mimics the gastric physiology of humans. A gerbil-adapted H. pylori strain, HP87 P7, showed energy-dependent behavior, while its isogenic tlpD mutant lost it. A TlpD ...[more]

PMID: 23836820

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Project description:BACKGROUND: The Mongolian gerbils are a good model to mimic the Helicobacter pylori-associated pathogenesis of the human stomach. In the current study the gerbil-adapted strain B8 was completely sequenced, annotated and compared to previous genomes, including the 73 supercontigs of the parental strain B128. RESULTS: The complete genome of H. pylori B8 was manually curated gene by gene, to assign as much function as possible. It consists of a circular chromosome of 1,673,997 bp and of a small plasmid of 6,032 bp carrying nine putative genes. The chromosome contains 1,711 coding sequences, 293 of which are strain-specific, coding mainly for hypothetical proteins, and a large plasticity zone containing a putative type-IV-secretion system and coding sequences with unknown function. The cag-pathogenicity island is rearranged such that the cagA-gene is located 13,730 bp downstream of the inverted gene cluster cagB-cag1. Directly adjacent to the cagA-gene, there are four hypothetical genes and one variable gene with a different codon usage compared to the rest of the H. pylori B8-genome. This indicates that these coding sequences might be acquired via horizontal gene transfer.The genome comparison of strain B8 to its parental strain B128 delivers 425 unique B8-proteins. Due to the fact that strain B128 was not fully sequenced and only automatically annotated, only 12 of these proteins are definitive singletons that might have been acquired during the gerbil-adaptation process of strain B128. CONCLUSION: Our sequence data and its analysis provide new insight into the high genetic diversity of H. pylori-strains. We have shown that the gerbil-adapted strain B8 has the potential to build, possibly by a high rate of mutation and recombination, a dynamic pool of genetic variants (e.g. fragmented genes and repetitive regions) required for the adaptation-processes. We hypothesize that these variants are essential for the colonization and persistence of strain B8 in the gerbil stomach during in ammation.

Dataset Information

Role of energy sensor TlpD of Helicobacter pylori in gerbil colonization and genome analyses after adaptation in the gerbil.

Publications

Role of energy sensor TlpD of Helicobacter pylori in gerbil colonization and genome analyses after adaptation in the gerbil.

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