Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes

Abstract

The compositions of bacterial genomes can be changed rapidly and dramatically through a variety of processes including horizontal gene transfer. This form of change is key to bacterial evolution, as it leads to 'evolution in quantum leaps'. Horizontal gene transfer entails the incorporation of genetic elements transferred from another organism-perhaps in an earlier generation-directly into the genome, where they form 'genomic islands', i.e. blocks of DNA with signatures of mobile genetic elements. Genomic islands whose functions increase bacterial fitness, either directly or indirectly, have most likely been positively selected and can be termed 'fitness islands'. Fitness islands can be divided into several subtypes: 'ecological islands' in environmental bacteria and 'saprophytic islands', 'symbiosis islands' or 'pathogenicity islands' (PAIs) in microorganisms that interact with living hosts. Here we discuss ways in which PAIs contribute to the pathogenic potency of bacteria, and the idea that genetic entities similar to genomic islands may also be present in the genomes of eukaryotes.

Fig. 1. Model of the DNA pools in the genomes of prokaryotes. The DNA elements comprising the core as well as the flexible gene pools are presented in the circles. Functions encoded by the pools are given in the lower part of the diagram.

Fig. 2. Schematic model of a genomic island of bacteria (upper part). The formerly transferred DNA block is linked to a tRNA gene and flanked by direct repeats (DR). The guanine plus cytosine (G+C) content of the genomic island is different from that of the core genome (lower part). Other abbreviations: int, integrase gene; abc, def and ghi, genes encoding specific functions; IS, insertion sequence element; bp, base pair.

Fig. 3. Model for the development of genomic islands. Following acquisition of transferred DNA and/or deletion of genetic material, a genomic island is selected. If the gene products of the island enhance the fitness of the recipient, the island-harboring bacteria will be positively selected. The gene products of these foreign blocks of DNA can contribute to survival in the environment, saprophytic life, symbiosis or pathogenicity.