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The Widespread Colonization Island of Actinobacillus actinomycetemcomitans

Abstract

Genomic islands, such as pathogenicity islands, contribute to the evolution and diversification of microbial life1. Here we report on the Widespread Colonization Island, which encompasses the tad (tight adherence) locus for colonization of surfaces and biofilm formation by the human pathogen Actinobacillus actinomycetemcomitans. At least 12 of the 14 genes at the tad locus are required for tenacious biofilm formation and synthesis of bundled Flp pili (fibrils) that mediate adherence. The pilin subunit2, Flp1, remains inside the cell in tad-locus mutants, indicating that these genes encode a secretion system for export and assembly of fibrils. We found tad-related regions in a wide variety of Bacterial and Archaeal species3, and their sequence characteristics indicate possible horizontal transfer. To test the hypothesis of horizontal transfer, we compared the phylogeny of the tad locus to a robust organismal phylogeny using statistical tests of congruence and tree reconciliation techniques. Our analysis strongly supports a complex history of gene shuffling by recombination and multiple horizontal transfers, duplications and losses. We present evidence for a specific horizontal transfer event leading to the establishment of this region as a determinant of disease.

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Figure 1: tad locus.
Figure 2: Phenotypes of tad mutants.
Figure 3: Pairwise ILD analysis and partitions.
Figure 4: Phylogenies and tanglegrams.
Figure 5: Reticulogram.

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Acknowledgements

We thank M. Charleston for early release of TreeMap2b and helpful discussion, I.N. Sarkar for computer assistance, the members of D.H. Figurski's, R.D.'s and D.H. Fine's laboratories for helpful comments and the multiple genome sequencing projects from which data were collected for this analysis. This work was funded by grants from the US National Institutes of Health (to D.H. Figurski and R.D.). R.D. is also supported by the Lewis B. and Dorothy Cullman Program for Molecular Systematics at the American Museum of Natural History. S.C.K. was partially supported by a training grant from the US National Institutes of Health to Columbia University. P.J.P. is supported by the Medical Scientist Training Program of Columbia University.

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Correspondence to David H Figurski.

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Planet, P., Kachlany, S., Fine, D. et al. The Widespread Colonization Island of Actinobacillus actinomycetemcomitans. Nat Genet 34, 193–198 (2003). https://doi.org/10.1038/ng1154

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