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The Widespread Colonization Island of Actinobacillus actinomycetemcomitans
Paul J Planet1, Scott C Kachlany, Daniel H Fine
1Department of Microbiology, College of Physicians & Surgeons, Columbia University, 701 West 168th Street, New York, New York 10032, USA.
Abstract:
Genomic islands, such as pathogenicity islands, contribute to the evolution and diversification of microbial life. 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 subunit, 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 species, 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.
Insights
The Widespread Colonization Island, containing the tight adherence (tad) locus, is crucial for biofilm formation and surface colonization in Actinobacillus actinomycetemcomitans. Its presence across diverse species suggests horizontal gene transfer played a role in its evolution and disease association.
Area of Science:
- Microbiology
- Genomics
- Evolutionary Biology
Background:
- Genomic islands drive microbial evolution and diversification.
- Pathogenicity islands are key examples of mobile genetic elements.
- The tight adherence (tad) locus is involved in surface colonization and biofilm formation.
Purpose of the Study:
- To investigate the Widespread Colonization Island and its tad locus in Actinobacillus actinomycetemcomitans.
- To determine the role of the tad locus genes in biofilm formation and pilus assembly.
- To explore the evolutionary history and distribution of tad-related regions in bacteria and archaea.
Main Methods:
- Genetic analysis of tad-locus mutants in Actinobacillus actinomycetemcomitans.
- Phylogenetic analysis comparing the tad locus to organismal phylogeny.
- Statistical tests of congruence and tree reconciliation to assess gene transfer events.
Main Results:
- At least 12 tad genes are essential for biofilm formation and bundled Flp pilus synthesis.
- The tad locus appears to encode a secretion system for Flp pilus export and assembly.
- Tad-related regions are widespread in Bacteria and Archaea, indicating horizontal gene transfer.
- Phylogenetic analysis supports a complex evolutionary history involving recombination, horizontal transfers, duplications, and losses.
Conclusions:
- The Widespread Colonization Island, encompassing the tad locus, is a significant factor in Actinobacillus actinomycetemcomitans colonization and pathogenesis.
- Evidence strongly supports multiple horizontal gene transfer events shaping the evolution of the tad locus.
- A specific horizontal transfer event likely contributed to the establishment of this region as a disease determinant.