Abstract
Genes encoding proteins in a common pathway are often found near each other along bacterial chromosomes. Several explanations have been proposed to account for the evolution of these structures. For instance, natural selection may directly favour gene clusters through a variety of mechanisms, such as increased efficiency of coregulation. An alternative and controversial hypothesis is the selfish operon model, which asserts that clustered arrangements of genes are more easily transferred to other species, thus improving the prospects for survival of the cluster. According to another hypothesis (the persistence model), genes that are in close proximity are less likely to be disrupted by deletions. Here we develop computational models to study the conditions under which gene clusters can evolve and persist. First, we examine the selfish operon model by re-implementing the simulation and running it under a wide range of conditions. Second, we introduce and study a Moran process in which there is natural selection for gene clustering and rearrangement occurs by genome inversion events. Finally, we develop and study a model that includes selection and inversion, which tracks the occurrence and fixation of rearrangements. Surprisingly, gene clusters fail to evolve under a wide range of conditions. Factors that promote the evolution of gene clusters include a low number of genes in the pathway, a high population size, and in the case of the selfish operon model, a high horizontal transfer rate. The computational analysis here has shown that the evolution of gene clusters can occur under both direct and indirect selection as long as certain conditions hold. Under these conditions the selfish operon model is still viable as an explanation for the evolution of gene clusters.
Highlights
A conspicuous feature of bacterial genomes is the grouping of genes involved in a metabolic pathway into functional units on the chromosome
Genes involved in a common pathway or function are frequently found near each other on bacterial chromosomes
A influential theory is the selfish operon model, which posits that horizontal transfer could promote gene clustering by favouring transfer of arrangements of genes that are close together
Summary
A conspicuous feature of bacterial genomes is the grouping of genes involved in a metabolic pathway into functional units on the chromosome. Linkage studies of Escherichia coli and Salmonella typhimurium showed that genes in the biosynthetic pathways of tryptophan and histidine occur on a contiguous region of the genome [1,2]. Gene clustering has since become recognized as a widespread feature of bacterial genomes. Regulatory genes have been found close to the genes they regulate. A classic example is the lacI repressor gene, which resides near but not within the lacZYA operon in Escherichia coli. The extent of gene clustering is variable – a given set of related genes may be clustered in one species but unclustered and/or reordered in another [6,7]. Most clusters do not contain much intergenic DNA, and in some cases genes even overlap [8,9]
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