The Widespread Colonization Island of Actinobacillus actinomycetemcomitans

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.

Complete genome sequence of Vibrio fischeri : A symbiotic bacterium with pathogenic congeners

“…Two of the remaining four pilus gene clusters are paralogs (one on each V. fischeri chromosome) that are homologous to the Flp1 type IV-B tight adhesion (tad) pilus family. Members of this evolutionarily diverse family are found in many bacteria (24), including V. parahaemolyticus and V. vulnificus, but not the sequenced V. cholerae strain. The last two type-IV pilus loci of V. fischeri have homologs only in V. cholerae: one encodes a highly diverged PilA-like gene (7), and the other is a toxincoregulated pilus (TCP)-encoding locus (25) (Fig.…”

Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model

“…Remarkably, tad-related loci are present in diverse Bacteria and Archaea, and we have proposed that the role of tad-like loci in other microbes is to mediate adherence in different environments (16). Recently, we have shown that the tad locus has a complex history that includes several horizontal transfer events between distant relatives, indicating that the region is a mobile genomic island, which we designated the Widespread Colonization Island (WCI) (20). In the case of A. actinomycetemcomitans and several other organisms, including Pasteurella multocida and Haemophilus ducreyi, the WCI appears to be a pathogenicity island (20).…”

“…The tight-adherence phenotype is thought to be important for colonization of host surfaces, and recently we reported that an adherent clinical isolate was able to colonize, survive, and persist in the oral cavity of rats (2). Using random transposon mutagenesis, we recently identified a tightadherence (tad) locus that contains 14 genes ( flp-1-flp-2-tadVrcpCAB-tadZABCDEFG), of which at least 12 are essential for tight nonspecific adherence, autoaggregation, and pili formation (16,20). The genes appear to be arranged in an operon.…”

tfoX (sxy)-dependent transformation of Aggregatibacter (Actinobacillus) actinomycetemcomitans

“…2A). tadE is a gene well within the tad locus ; no USSs were found in a search of the 14-kb tad locus sequence from strains HK1651 (Roe et al, 2006) or CU1000 (Planet et al, 2003).…”

“…The three natural methods for gene transfer (transformation, conjugation, and transduction) have all been observed in A. actinomycetemcomitans (Tϕnjum et al, 1990;Goncharoff et al, 1993;Willi et al, 1997;Galli et al, 2001). We previously developed an efficient method for conjugationbased transposon-insertion mutagenesis (Thomson et al, 1999) that allowed us to isolate three independent mutations in the catalase gene (katA) of A. actinomycetemcomitans (Thomson et al, 1999) and in genes involved in non-specific adherence (Kachlany et al, , 2001bPlanet et al, 2003). For the latter, we identified the tad (tight adherence) locus, which encodes a novel secretion system responsible for the synthesis, assembly, and secretion of bundled type IVb pili, termed Flp fibrils (Kachlany et al, 2001a).…”