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Plastic cells and populations: DNA substrate characteristics in Helicobacter pylori transformation define a flexible but conservative system for genomic variation

Steven M. Levine^*, Edward A. Lin^*, Walid Emara^*, Josephine Kang^*, Michael DiBenedetto^*, Takafumi Ando, Daniel Falush and Martin J. Blaser^*,,1

Departments of
^* Medicine and

Microbiology, New York University School of Medicine, New York, New York, USA;

Department of Gastroenterology, Nagoya University Graduate School of Medicine, Nagoya, Japan; and

Department of Statistics, Peter Medawar Building for Pathogen Research, Oxford, UK

¹Correspondence: Dept. of Medicine, 550 First Ave., New York, NY 10016, USA. E-mail: martin.blaser{at}med.nyu.edu

Helicobacter pylori, bacteria that colonize the human gastric mucosa, are naturally competent for transformation by exogenous DNA, and show a panmictic population structure. To understand the mechanisms involved in its horizontal gene transfer, we sought to define the interval required from exposure to substrate DNA until DNA uptake and expression of a selectable phenotype, as well as the relationship of transforming fragment length, concentration, homology, symmetry, and strandedness, to the transformation frequency. We provide evidence that natural transformation in H. pylori differs in efficiency among wild-type strains but is saturable and varies with substrate DNA length, symmetry, strandedness, and species origin. We show that H. pylori cells can be transformed within one minute of contact with DNA, by DNA fragments as small as 50 bp, and as few as 5 bp on one flank of a selectable single nucleotide mutation is sufficient substrate for recombination of a transforming fragment, and that double-stranded DNA is the preferred (1000-fold >single-stranded) substrate. The high efficiency of double-stranded DNA as transformation substrate, in conjunction with strain-specific restriction endonucleases suggests a model of short-fragment recombination favoring closest relatives, consistent with the observed H. pylori population biology.—Levine, S. M., Lin, E. A., Emara, W., Kang, J., DiBenedetto, M., Ando, T., Falush, D., Blaser, M. J. Plastic cells and populations: DNA substrate characteristics in Helicobacter pylori transformation define a flexible but conservative system for genomic variation.

Key Words: bacterial genetics • microbiology • pathogenesis • molecular biology • colonization • microbial diversity

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