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Insights and inferences about integron evolution from genomic data

Abstract

Background

Integrons are mechanisms that facilitate horizontal gene transfer, allowing bacteria to integrate and express foreign DNA. These are important in the exchange of antibiotic resistance determinants, but can also transfer a diverse suite of genes unrelated to pathogenicity. Here, we provide a systematic analysis of the distribution and diversity of integron intI genes and integron-containing bacteria.

Results

We found integrons in 103 different pathogenic and non-pathogenic bacteria, in six major phyla. Integrons were widely scattered, and their presence was not confined to specific clades within bacterial orders. Nearly 1/3 of the intI genes that we identified were pseudogenes, containing either an internal stop codon or a frameshift mutation that would render the protein product non-functional. Additionally, 20% of bacteria contained more than one integrase gene. dN/dS ratios revealed mutational hotspots in clades of Vibrio and Shewanella intI genes. Finally, we characterized the gene cassettes associated with integrons in Methylobacillus flagellatus KT and Dechloromonas aromatica RCB, and found a heavy metal efflux gene as well as genes involved in protein folding and stability.

Conclusion

Our analysis suggests that the present distribution of integrons is due to multiple losses and gene transfer events. While, in some cases, the ability to integrate and excise foreign DNA may be selectively advantageous, the gain, loss, or rearrangment of gene cassettes could also be deleterious, selecting against functional integrases. Thus, such a high fraction of pseudogenes may suggest that the selective impact of integrons on genomes is variable, oscillating between beneficial and deleterious, possibly depending on environmental conditions.

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