The Tryptophanase Gene Cluster of Haemophilus influenzae Type b: Evidence for Horizontal Gene Transfer

Abstract

Among strains of Haemophilus influenzae, the ability to catabolize tryptophan (as detected by indole production) varies and is correlated with pathogenicity. Tryptophan catabolism is widespread (70 to 75%) among harmless respiratory isolates but is nearly universal (94 to 100%) among strains causing serious disease, including meningitis. As a first step in investigating the relationship between tryptophan catabolism and virulence, we have identified genes in pathogenic H. influenzae which are homologous to the tryptophanase (tna) operon of Escherichia coli. The tna genes are located on a 3.1-kb fragment betweennlpD and mutS in the H. influenzaetype b (Eagan) genome, are flanked by 43-bp direct repeats of an uptake signal sequence downstream from nlpD, and appear to have been inserted as a mobile unit within this sequence. The organization of this insertion is reminiscent of pathogenicity islands. Thetna cluster is found at the same map location in all indole-positive strains of H. influenzae surveyed and is absent from reference type d and e genomes. In contrast to H. influenzae, most other Haemophilus species lacktna genes. Phylogenetic comparisons suggest that thetna cluster was acquired by intergeneric lateral transfer, either by H. influenzae or a recent ancestor, and thatE. coli may have acquired its tnaA gene from a related source. Genomes of virulent H. influenzae resemble those of pathogenic enterics in having an island of laterally transferred DNA next to mutS.

Indole as an intercellular signal in microbial communities

“…Additionally, among isolates of H. influenzae, most serotypes (94-100%) are indole-positive, compared with only 70-75% of harmless isolates. The result indicates that indole production is necessary but not sufficient for virulence to this strain (Martin et al, 1998).…”

Prevalence of RNA polymerase stalling at Escherichia coli promoters after open complex formation

“…Such pause-mediated transcription repression might fine-tune gene expression, keeping transcription rates more uniform, and contributing to other types of regulation, such as metabolic control by Crp at the tnaA promoter (Deeley and Yanofsky, 1982) and tryptophan-induced attenuation in the tnaA leader (Konan and Yanofsky, 2000;Gong and Yanofsky, 2001). Potential pause-inducing sequences also span the tnaA leaders of Enterobacter aerogenes SM-18 (Kawasaki, Yokota et al, 1993), Haemophilus influenzae (Martin et al, 1998) and Proteus vulgaris (Kamath and Yanofsky, 1992), suggesting an important conserved function.…”

Microbial volatile compounds in health and disease conditions

“…Indole production from tryptophan is a property of a number of different microbial species including; E. coli (Newton and Snell 1964), Proteus vulgaris (Kamath and Yanofsky 1992), Haemophilus influenzae (Martin et al 1998), Porphyromonas gingivalis (Yoshida et al 2009) and F. nucleatum (Imamura et al 2010). The enzyme responsible is tryptophanase (more correctly named as tryptophan indole-lyase; EC4.1.99.1) and it transforms tryptophan into indole, pyruvate and ammonium ion (figure 2, Newton and Snell 1964).…”