Genomic islands: tools of bacterial horizontal gene transfer and evolution

Abstract

Bacterial genomes evolve through mutations, rearrangements or horizontal gene transfer. Besides the core genes encoding essential metabolic functions, bacterial genomes also harbour a number of accessory genes acquired by horizontal gene transfer that might be beneficial under certain environmental conditions. The horizontal gene transfer contributes to the diversification and adaptation of microorganisms, thus having an impact on the genome plasticity. A significant part of the horizontal gene transfer is or has been facilitated by genomic islands (GEIs). GEIs are discrete DNA segments, some of which are mobile and others which are not, or are no longer mobile, which differ among closely related strains. A number of GEIs are capable of integration into the chromosome of the host, excision, and transfer to a new host by transformation, conjugation or transduction. GEIs play a crucial role in the evolution of a broad spectrum of bacteria as they are involved in the dissemination of variable genes, including antibiotic resistance and virulence genes leading to generation of hospital 'superbugs', as well as catabolic genes leading to formation of new metabolic pathways. Depending on the composition of gene modules, the same type of GEIs can promote survival of pathogenic as well as environmental bacteria.

Fig. 1

General features of GEIs. GEIs are relatively large segments of DNA whose nucleotide characteristics often differ from the rest of the chromosome. GEIs are often inserted at tRNA genes and flanked by DR. GEIs typically harbour genes encoding factors involved in genetic mobility, such as integrases, transposases and insertion sequences (IS). According to their gene content, GEIs can be described as pathogenicity, symbiosis, metabolic, fitness or resistance islands.

Fig. 2

Variable types of GEIs. GEIs come in a large spectrum of varieties and encompass other categories of elements, such as conjugative transposons/ICEs, integrated plasmids, nonreplicative but excisable elements, and cryptic or damaged prophages. Grey-shaded areas point to self-mobile GEIs.

Fig. 3

Integration, development and excision of GEIs. The schematic life-style of mobile GEI consists of the following steps: (1) acquisition by horizontal gene transfer; (2) integration into the host's chromosome by site-specific recombination; (3) development of the GEI by genetic rearrangements, gene loss (a) or gene acquisition (b); (4) excision from the chromosome; (5) transfer to another recipient.

Fig. 4

Various functions encoded by GEIs of the same family. Modified Artemis Comparison Tool view of four GEIs of the same family: ICEHin1056, clc, ICEHpaT3T1 and PAPI. Homologous sequences (minimum cut-off=50) are indicated by grey lines joining regions of the four GEIs. Gene modules homologous in all shown GEIs are represented by white boxes, and modules specific for individual GEIs by black boxes. The figure shows that depending on the composition of gene modules, members of the same family of GEIs can promote survival of pathogenic (ICEHin1056, ICEHpaT3T1, PAPI of Haemophilus influenzae, Haemophilus parainfluenzae and Pseudomonas aeruginosa, respectively) as well as environmental (clc of Pseudomonas sp. B13) bacteria. ATB resist., antibiotics resistance; T4SS, type IV secretion system; Integr., integration.