Extensive repetitive DNA facilitates prokaryotic genome plasticity

Abstract

Prokaryotic genomes are substantially diverse, even when from closely related species, with the resulting phenotypic diversity representing a repertoire of adaptations to specific constraints. Within the microbial population, genome content may not be fixed, as changing selective forces favor particular phenotypes; however, organisms well adapted to particular niches may have evolved mechanisms to facilitate such plasticity. The highly diverse Helicobacter pylori is a model for studying genome plasticity in the colonization of individual hosts. For H. pylori, neither point mutation, nor intergenic recombination requiring the presence of multiple colonizing strains, is sufficient to fully explain the observed diversity. Here we demonstrate that H. pylori has extensive, nonrandomly distributed repetitive chromosomal sequences, and that recombination between identical repeats contributes to the variation within individual hosts. That H. pylori is representative of prokaryotes, especially those with smaller (<2 megabases) genomes, that have similarly extensive direct repeats, suggests that recombination between such direct DNA repeats is a widely conserved mechanism to promote genome diversification. P rokaryotes that successfully colonize niches for extended periods of time must be capable of adapting to changing environmental stresses (1). Genomic diversity, caused by spontaneous point mutation, intragenomic rearrangement, and horizontal gene acquisition (2), creates a phenotypically diverse population from which the most-fit variants are selected. Colonization of the primate stomach by Helicobacter pylori is prolonged, usually persisting for decades without host clearance (3). That essentially all H. pylori isolates obtained from unrelated individuals are genetically distinguishable (4), and that diverse subclones have been identified in individual hosts (5-7) suggest that persistence may be facilitated by the organism's ability to adapt to dynamic environments by continuous change (8). HIV and other pathogenic viruses that persistently infect hosts employ similar strategies of ''quasispecies'' development to increase fitness success (9).For H. pylori, neither spontaneous point mutation (10) nor recombination with other bacterial cells (11) is sufficient to explain observed intrahost genetic variation (5, 7). Computational analysis of the fully sequenced H. pylori strain 26695 (12) indicates numerous direct DNA repeats (13, 14); however, these studies do not demonstrate a role for repeats through experimental analyses, provide evidence that these repeat structures are involved in any biologic function, or assess how the nonrandom distribution of repeats may affect the physiology or evolution of the host organism. Because recombination involving direct repeats allows for deletion or duplication of intervening sequences (15), we sought to determine the extent to which H. pylori uses repetitive DNA sequences to generate diversity. Our observations provide evidence that the presence of extensive, nonrandomly distribu...

A Recombination Puzzle Solved: Role for New DNA Repair Systems in Helicobacter pylori Diversity/Persistence

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Temporal and Spatial Scaling of the Genetic Structure of a Vector-Borne Plant Pathogen

“…As a consequence, the rate with which these errors occur varies in a locus-specific manner and is several orders of magnitude higher than point mutations in nonrepeat DNA regions (18). Bacterial repeats in protein coding or upstream of regulatory regions are responsible for phenotypic switches as well as cell adaptations to specific environmental challenges (3,32). Here, most SSRs were located in housekeeping genes, noncoding regions, and hypothetical proteins (14,31).…”

The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: Evolution during disease progression

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