Academic journal article Genetics

Patterns of Sequence Divergence in 5' Intergenic Spacers and Linked Coding Regions in 10 Species of Pathogenic Bacteria Reveal Distinct Recombinational Histories

Academic journal article Genetics

Patterns of Sequence Divergence in 5' Intergenic Spacers and Linked Coding Regions in 10 Species of Pathogenic Bacteria Reveal Distinct Recombinational Histories

Article excerpt


We compared the pattern of nucleotide difference in 8034 genes and in their 5' intergenic spacers between conspecific pairs of genomes from 10 species of pathogenic bacteria. Certain genes or spacers showed much greater sequence divergence between the genotypes compared to others; such divergent regions plausibly originated by recombinational events by which a gene and/or spacers was donated from a divergent genome. Different patterns of divergence in genes and spacers identified different recombinational patterns. For example, in Chlamydophila pneumoniae, there were examples of both unusually divergent spacers and unusually divergent genes, but there were no cases in which a gene and its spacer were both unusually divergent. This pattern suggests that, in C. pneumoniae, recombination events have broken up the linkage between genes and 5' spacers. By contrast, in Streptococcus agalactiae, there were a number of cases in which both spacer and gene were unusually divergent, indicating that a number of large-scale recombination events that included both genes and 5' spacers have occurred; there was evidence of at least two large-scale recombination events in the genomic region including the pur genes in S. agalactiae.

THE extent to which recombination occurs in free-living bacterial populations is an important factor in their population biology. In the case of pathogenic bacteria, FEIL et al. (2000) argue that an understanding of the role of recombination is important for prophylaxis and treatment because recombination will have a major impact on the evolution of pathogenicity and the effectiveness of vaccines. Classical studies, using techniques such as multilocus enzyme electrophoresis, assessed recombination between protein-coding loci (SELANDER et al. 1986). More recently, studies focused on sequence data have tested for evidence of small-scale intralocus recombinational events (MCGRAW et al. 1999). However, little attention has been paid to the extent of recombination between protein-coding loci and adjacent intergenic (spacer) regions.

Intergenic regions in prokaryotes are much shorter on average than those of eukaryotes, and consequently the density of regulatory elements per intergenic region is expected to be much higher in prokaryotes than in eukaryotes (ROGOZIN et al. 2002). Spacers between genes in a head-to-head orientation will include promoters for both genes, while spacers between genes in a head-to-tail orientation will include the promoter of one gene. Consequently, the extent of recombination between genes and adjacent spacers may be an important factor in the evolution of intraspecific differences in gene regulation.

A number of recent reviews have focused on the need to understand the evolutionary dynamics of promoters and other genomic regions involved in the regulation of gene expression (RODRIGUEZ-TRELLES et al. 2003; WRAY et al. 2003). Promoter sequences required for gene expression are expected to be subject to purifying selection (KOHN et al. 2004). Alternatively, there is evidence that natural selection may favor differentiation of promoter regions between populations within species (ROCKMAN et al. 2003) or between closely related species (KOHN et al. 2004) when environmental differences favor changes in the pattern of gene expression. In bacteria, a number of studies have analyzed genome-wide patterns of nucleotide substitution in protein-coding genes by comparing conspecific genomic sequences (HUGHES et al. 2002; JORDAN et al. 2002). This approach has not been extended to intergenic spacers except in a recent study by FUGLSANG (2004) analyzing the 50 nucleotides upstream of start codons and downstream of stop codons in Escherichia coli and two related species.

Here we analyze patterns of nucleotide difference in 5' intergenic spacers and linked protein-coding genes by comparing conspecific genomic sequences from 10 species of pathogenic bacteria. This data set enables us to compare the pattern of sequence differentiation in intergenic regions with that in protein-coding genes. …

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