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Gain and Loss of Multiple Genes During the Evolution of Helicobacter pylori

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      Abstract

      Sequence diversity and gene content distinguish most isolates of Helicobacter pylori. Even greater sequence differences differentiate distinct populations of H. pylori from different continents, but it was not clear whether these populations also differ in gene content. To address this question, we tested 56 globally representative strains of H. pylori and four strains of Helicobacter acinonychis with whole genome microarrays. Of the weighted average of 1,531 genes present in the two sequenced genomes, 25% are absent in at least one strain of H. pylori and 21% were absent or variable in H. acinonychis. We extrapolate that the core genome present in all isolates of H. pylori contains 1,111 genes. Variable genes tend to be small and possess unusual GC content; many of them have probably been imported by horizontal gene transfer. Phylogenetic trees based on the microarray data differ from those based on sequences of seven genes from the core genome. These discrepancies are due to homoplasies resulting from independent gene loss by deletion or recombination in multiple strains, which distort phylogenetic patterns. The patterns of these discrepancies versus population structure allow a reconstruction of the timing of the acquisition of variable genes within this species. Variable genes that are located within the cag pathogenicity island were apparently first acquired en bloc after speciation. In contrast, most other variable genes are of unknown function or encode restriction/modification enzymes, transposases, or outer membrane proteins. These seem to have been acquired prior to speciation of H. pylori and were subsequently lost by convergent evolution within individual strains. Thus, the use of microarrays can reveal patterns of gene gain or loss when examined within a phylogenetic context that is based on sequences of core genes.

      Abstract

      SynopsisThe Gram-negative pathogenic bacterium Helicobacter pylori colonizes the stomach of 50% of mankind and has probably infected humans since their origins. Due to geographic isolation and frequent local recombination, phylogeographic differences within H. pylori have arisen, resulting in multiple populations and subpopulations that mirror ancient human migrations and genetic diversity. We have examined the gene content of representatives of these populations by whole genome microarrays. Only 1,111 genes are predicted to exist in all H. pylori of the 1,531 that are present on average in two sequenced genomes. Missing genes fall into two classes: one class contains genes within the cag pathogenicity island that was acquired en bloc after speciation and is present only in particular populations. The second class contains a variety of genes whose function may be unimportant for the cell and that were acquired prior to speciation. Their absence in individual isolates reflects convergent evolution through gene loss. Thus, patterns of gene gain or loss can be identified by whole genome microarrays within a phylogenetic context that can be supplied by sequences of genes from the core genome.

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      Most cited references 61

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      ACT: the Artemis Comparison Tool.

      The Artemis Comparison Tool (ACT) allows an interactive visualisation of comparisons between complete genome sequences and associated annotations. The comparison data can be generated with several different programs; BLASTN, TBLASTX or Mummer comparisons between genomic DNA sequences, or orthologue tables generated by reciprocal FASTA comparison between protein sets. It is possible to identify regions of similarity, insertions and rearrangements at any level from the whole genome to base-pair differences. ACT uses Artemis components to display the sequences and so inherits powerful searching and analysis tools. ACT is part of the Artemis distribution and is similarly open source, written in Java and can run on any Java enabled platform, including UNIX, Macintosh and Windows.
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        The complete genome sequence of the gastric pathogen Helicobacter pylori.

        Helicobacter pylori, strain 26695, has a circular genome of 1,667,867 base pairs and 1,590 predicted coding sequences. Sequence analysis indicates that H. pylori has well-developed systems for motility, for scavenging iron, and for DNA restriction and modification. Many putative adhesins, lipoproteins and other outer membrane proteins were identified, underscoring the potential complexity of host-pathogen interaction. Based on the large number of sequence-related genes encoding outer membrane proteins and the presence of homopolymeric tracts and dinucleotide repeats in coding sequences, H. pylori, like several other mucosal pathogens, probably uses recombination and slipped-strand mispairing within repeats as mechanisms for antigenic variation and adaptive evolution. Consistent with its restricted niche, H. pylori has a few regulatory networks, and a limited metabolic repertoire and biosynthetic capacity. Its survival in acid conditions depends, in part, on its ability to establish a positive inside-membrane potential in low pH.
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          Helicobacter pylori infection.

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            Author and article information

            Affiliations
            [1 ] Department of Molecular Biology, Max-Planck-Institut für Infektionsbiologie, Berlin, Germany
            [2 ] Institut für Medizinische Mikrobiologie, Justus-Liebig-Universität, Giessen, Germany
            [3 ] Core Facility Bioinformatics, Max-Planck-Institut für Infektionsbiologie, Berlin, Germany
            [4 ] Functional Genomics Center Zurich, ETH Zurich/University of Zurich, Zurich, Switzerland
            [5 ] Department of Medicine, M.E. DeBakey Veterans Affairs Medical Center and Baylor College of Medicine, Houston, Texas, United States of America
            [6 ] Medizinische Hochschule Hannover, Institut für Medizinische Mikrobiologie und Krankenhaushygiene, Hannover, Germany
            National Institute of Genetics, Japan
            Author notes
            * To whom correspondence should be addressed. E-mail: achtman@ 123456mpiib-berlin.mpg.de
            Contributors
            Role: Editor
            Journal
            PLoS Genet
            pgen
            PLoS Genetics
            Public Library of Science (San Francisco, USA )
            1553-7390
            1553-7404
            October 2005
            7 October 2005
            : 1
            : 4
            1245399
            10.1371/journal.pgen.0010043
            05-PLGE-RA-0110R1 plge-01-04-01
            16217547
            (Editor)
            Copyright: © 2005 Gressmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
            Categories
            Research Article
            Evolution
            Infectious Diseases
            Microbiology
            Genetics/Genomics
            Genetics/Population Genetics
            Genetics/Comparative Genomics
            Eubacteria
            Custom metadata
            Gressmann H, Linz B, Ghai R, Pleissner KP, Schlapbach R, et al. (2005) Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 1(4): e43.

            Genetics

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