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Genomic islands in pathogenic and environmental microorganisms

Key Points

  • Genomic islands (GEIs) are characterized by their large size (>10 kb), their frequent association with tRNA-encoding genes and a different G+C content compared with the rest of the chromosome. Many genomic islands are flanked by repeat structures and carry fragments of other mobile and accessory genetic elements, such as bacteriophages, plasmids and insertion sequence (IS) elements.

  • Some GEIs can excise themselves spontaneously from the chromosome and can be transferred to other suitable recipients. GEIs contribute to bacterial genome plasticity and, together with other mobile and accessory genetic elements, to the 'horizontal gene pool' of a given bacterial population.

  • A hypothetical 'life cycle' of GEIs includes the insertion of mobile genetic elements into the bacterial chromosome. Through rearrangements and consecutive insertion and deletion events, the organization and gene content of the original element becomes modified and can lose the features of mobile elements. Owing to the action of bacteriophage integrases that are encoded on genomic islands, these genetic elements can be deleted from the chromosome and, upon transfer into a suitable host, can be chromosomally inserted by site-specific recombination.

  • GEIs contribute to fitness and adaptation. GEIs typically provide a gain-of-function to the host bacterium. As GEIs promote the transfer of multi-gene families, entire phenotypes can be changed in a single-step gene-transfer event.

  • GEIs are expected to have a role in ecological niches where microbial cell numbers and diversity are high and/or in environments that are constantly changing. The GEIs identified so far are relevant in the context of pathogenicity, symbiosis, antibiotic resistance, xenobiotic degradation, and primary and secondary metabolism. It is expected that the functional diversity of GEIs is even greater than is currently known.

  • As GEIs are widely distributed in pathogenic, non-pathogenic and environmental microorganisms, they represent a paradigm rather than a paradox for microbial evolution, underlining the importance of horizontal gene transfer in this process.

Abstract

Horizontal gene transfer is an important mechanism for the evolution of microbial genomes. Pathogenicity islands — mobile genetic elements that contribute to rapid changes in virulence potential — are known to have contributed to genome evolution by horizontal gene transfer in many bacterial pathogens. Increasing evidence indicates that equivalent elements in non-pathogenic species — genomic islands — are important in the evolution of these bacteria, influencing traits such as antibiotic resistance, symbiosis and fitness, and adaptation in general. This review discusses the recent lessons that have been learned from pathogenicity islands in pathogenic microorganisms and how they apply to the role of genomic islands in commensal, symbiotic and environmental bacteria.

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Figure 1: Evolution of bacterial variants by acquisition and loss of genetic information.
Figure 2: General characteristics of genomic islands.
Figure 3: Hypothetical 'life cycle' of genomic islands.

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Acknowledgements

We thank H. Merkert for excellent graphical assistance. Our own work related to the topic is supported by the Deutsche Forschungsgemeinschaft, the Bundesministerium für Bildung und Forschung, the Fonds der Chemischen Industrie and the Bavarian Research Foundation.

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Correspondence to Jörg Hacker.

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DATABASES

Entrez

Bradyrhizobium japonicum strain USDA110

Campylobacter jejuni

CTnscr94

Escherichia coli

Haemophilus influenzae

Helicobacter pylori

Lactobacillus gasseri

Lactobacillus johnsonii strain NCC533

pHG1

Photorhabdus luminescens

Pseudomonas aeruginosa

Pseudomonas putida KT2440

Pseudomonas syringae

pSymA

pSymB

Staphylococcus aureus

Streptomyces avermitilis

Streptomyces coelicolor

Thermotoga maritima

Ti plasmid

Wolinella succinogenes

Xylella fastidiosa

FURTHER INFORMATION

Genomic island database

Pathogenic enterobacteria laboratory, University of Würzburg

Microbial diversity laboratory, University of Würzburg

Glossary

SUBTRACTION HYBRIDIZATION

A technique that is used to specifically enrich the DNA species that are present in one sample but not in another by hybridizing the nucleic acids of the two samples and removing the associated double-stranded molecules.

SYNTENY

The property of being located on the same chromosome. In bacteria, chromosomal regions with conserved synteny represent dna segments in which the gene order is conserved in different species.

POLYKETIDE

A natural product that is assembled from malonyl CoA units through intermediates with many ketone groups (polyketonic) that allow for directed reactivity to product structures. Polyketides represent an important class of secondary metabolites that include many medicinal and antibiotic compounds.

T-DNA

A DNA segment of the tumour-inducing (Ti) plasmid of A. tumefaciens. It is transferred into the nuclei of infected cells where it is stably integrated into the host genome and transcribed, causing crown gall disease. T-DNA contains two types of genes: oncogenes that encode enzymes involved in the synthesis of auxins and cytokinins, which are responsible for tumour formation; and genes coding for the synthesis of opines.

OPINE FOOD SUBSTRATES

Compounds produced by condensation between amino acids and sugars. They are synthesized and excreted by crown-gall cells and consumed by A. tumefaciens as carbon and nitrogen sources. Opines are not easily catabolized by other bacterial species and allow A. tumefaciens to benefit from the production of plant opines.

NOD FACTOR

Bacterially produced substituted lipooligosaccharides that affect plant development in a host-specific way. They switch on a developmental pathway within the plant that triggers early features of nodule organogenesis in the rhizobium–legume symbiosis.

COLICINS

Polypeptide toxins produced by and active against Escherichia coli and closely related bacteria.

METAGENOMICS

The genomic analysis of all microorganisms present in a specific habitat.

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Dobrindt, U., Hochhut, B., Hentschel, U. et al. Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2, 414–424 (2004). https://doi.org/10.1038/nrmicro884

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