This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Martin, K.
Right arrow Articles by Golomb, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Martin, K.
Right arrow Articles by Golomb, M.

 Previous Article  |  Next Article 

J. Bacteriol., 01 1998, 107-118, Vol 180, No. 1
Copyright © 1998, American Society for Microbiology

The tryptophanase gene cluster of Haemophilus influenzae type b: evidence for horizontal gene transfer [In Process Citation]

K Martin, G Morlin, A Smith, A Nordyke, A Eisenstark and M Golomb
Division of Biological Sciences, University of Missouri, Columbia 65211, USA.

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 between nlpD and mutS in the H. influenzae type 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. The tna 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 lack tna genes. Phylogenetic comparisons suggest that the tna cluster was acquired by intergeneric lateral transfer, either by H. influenzae or a recent ancestor, and that E. 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.


This article has been cited by other articles:

  • Yoshida, Y., Sasaki, T., Ito, S., Tamura, H., Kunimatsu, K., Kato, H. (2009). Identification and molecular characterization of tryptophanase encoded by tnaA in Porphyromonas gingivalis. Microbiology 155: 968-978 [Abstract] [Full Text]  
  • Satola, S. W., Napier, B., Farley, M. M. (2008). Association of IS1016 with the hia Adhesin Gene and Biotypes V and I in Invasive Nontypeable Haemophilus influenzae. Infect. Immun. 76: 5221-5227 [Abstract] [Full Text]  
  • Erwin, A. L., Sandstedt, S. A., Bonthuis, P. J., Geelhood, J. L., Nelson, K. L., Unrath, W. C. T., Diggle, M. A., Theodore, M. J., Pleatman, C. R., Mothershed, E. A., Sacchi, C. T., Mayer, L. W., Gilsdorf, J. R., Smith, A. L. (2008). Analysis of Genetic Relatedness of Haemophilus influenzae Isolates by Multilocus Sequence Typing. J. Bacteriol. 190: 1473-1483 [Abstract] [Full Text]  
  • Takahata, S., Ida, T., Senju, N., Sanbongi, Y., Miyata, A., Maebashi, K., Hoshiko, S. (2007). Horizontal Gene Transfer of ftsI, Encoding Penicillin-Binding Protein 3, in Haemophilus influenzae. Antimicrob. Agents Chemother. 51: 1589-1595 [Abstract] [Full Text]  
  • Kobayashi, A., Hirakawa, H., Hirata, T., Nishino, K., Yamaguchi, A. (2006). Growth Phase-Dependent Expression of Drug Exporters in Escherichia coli and Its Contribution to Drug Tolerance.. J. Bacteriol. 188: 5693-5703 [Abstract] [Full Text]  
  • Erwin, A. L., Bonthuis, P. J., Geelhood, J. L., Nelson, K. L., McCrea, K. W., Gilsdorf, J. R., Smith, A. L. (2006). Heterogeneity in Tandem Octanucleotides within Haemophilus influenzae Lipopolysaccharide Biosynthetic Gene losA Affects Serum Resistance.. Infect. Immun. 74: 3408-3414 [Abstract] [Full Text]  
  • Fitzpatrick, D. A., Creevey, C. J., McInerney, J. O. (2006). Genome Phylogenies Indicate a Meaningful {alpha}-Proteobacterial Phylogeny and Support a Grouping of the Mitochondria with the Rickettsiales. Mol Biol Evol 23: 74-85 [Abstract] [Full Text]  
  • Erwin, A. L., Nelson, K. L., Mhlanga-Mutangadura, T., Bonthuis, P. J., Geelhood, J. L., Morlin, G., Unrath, W. C. T., Campos, J., Crook, D. W., Farley, M. M., Henderson, F. W., Jacobs, R. F., Muhlemann, K., Satola, S. W., van Alphen, L., Golomb, M., Smith, A. L. (2005). Characterization of Genetic and Phenotypic Diversity of Invasive Nontypeable Haemophilus influenzae. Infect. Immun. 73: 5853-5863 [Abstract] [Full Text]  
  • Gladitz, J., Shen, K., Antalis, P., Hu, F. Z., Post, J. C., Ehrlich, G. D. (2005). Codon usage comparison of novel genes in clinical isolates of Haemophilus influenzae. Nucleic Acids Res 33: 3644-3658 [Abstract] [Full Text]  
  • Shen, K., Antalis, P., Gladitz, J., Sayeed, S., Ahmed, A., Yu, S., Hayes, J., Johnson, S., Dice, B., Dopico, R., Keefe, R., Janto, B., Chong, W., Goodwin, J., Wadowsky, R. M., Erdos, G., Post, J. C., Ehrlich, G. D., Hu, F. Z. (2005). Identification, Distribution, and Expression of Novel Genes in 10 Clinical Isolates of Nontypeable Haemophilus influenzae. Infect. Immun. 73: 3479-3491 [Abstract] [Full Text]  
  • Watson, M. E. Jr, Burns, J. L., Smith, A. L. (2004). Hypermutable Haemophilus influenzae with mutations in mutS are found in cystic fibrosis sputum. Microbiology 150: 2947-2958 [Abstract] [Full Text]  
  • Gilsdorf, J. R., Marrs, C. F., Foxman, B. (2004). Haemophilus influenzae: Genetic Variability and Natural Selection To Identify Virulence Factors. Infect. Immun. 72: 2457-2461 [Full Text]  
  • Munson, R. S. Jr., Harrison, A., Gillaspy, A., Ray, W. C., Carson, M., Armbruster, D., Gipson, J., Gipson, M., Johnson, L., Lewis, L., Dyer, D. W., Bakaletz, L. O. (2004). Partial Analysis of the Genomes of Two Nontypeable Haemophilus influenzae Otitis Media Isolates. Infect. Immun. 72: 3002-3010 [Abstract] [Full Text]  
  • Li, Y., Altman, S. (2003). A specific endoribonuclease, RNase P, affects gene expression of polycistronic operon mRNAs. Proc. Natl. Acad. Sci. USA 100: 13213-13218 [Abstract] [Full Text]  
  • Androutsellis-Theotokis, A., Goldberg, N. R., Ueda, K., Beppu, T., Beckman, M. L., Das, S., Javitch, J. A., Rudnick, G. (2003). Characterization of a Functional Bacterial Homologue of Sodium-dependent Neurotransmitter Transporters. J. Biol. Chem. 278: 12703-12709 [Abstract] [Full Text]  
  • Daines, D. A., Cohn, L. A., Coleman, H. N., Kim, K. S., Smith, A. L. (2003). Haemophilus influenzae Rd KW20 has virulence properties. J Med Microbiol 52: 277-282 [Abstract] [Full Text]  
  • Bergman, N. H., Akerley, B. J. (2003). Position-Based Scanning for Comparative Genomics and Identification of Genetic Islands in Haemophilus influenzae Type b. Infect. Immun. 71: 1098-1108 [Abstract] [Full Text]  
  • Kotewicz, M. L., Li, B., Levy, D. D., LeClerc, J. E., Shifflet, A. W., Cebula, T. A. (2002). Evolution of multi-gene segments in the mutS-rpoS intergenic region of Salmonella enterica serovar Typhimurium LT2. Microbiology 148: 2531-2540 [Abstract] [Full Text]  
  • Davis, J., Smith, A. L., Hughes, W. R., Golomb, M. (2001). Evolution of an Autotransporter: Domain Shuffling and Lateral Transfer from Pathogenic Haemophilus to Neisseria. J. Bacteriol. 183: 4626-4635 [Abstract] [Full Text]  
  • Read, T. D., Satola, S. W., Farley, M. M. (2000). Nucleotide Sequence Analysis of Hypervariable Junctions of Haemophilus influenzae Pilus Gene Clusters. Infect. Immun. 68: 6896-6902 [Abstract] [Full Text]  
  • Konan, K. V., Yanofsky, C. (2000). Rho-Dependent Transcription Termination in the tna Operon of Escherichia coli: Roles of the boxA Sequence and the rut Site. J. Bacteriol. 182: 3981-3988 [Abstract] [Full Text]  
  • Chang, C.-C., Gilsdorf, J. R., DiRita, V. J., Marrs, C. F. (2000). Identification and Genetic Characterization of Haemophilus influenzae Genetic Island 1. Infect. Immun. 68: 2630-2637 [Abstract] [Full Text]  
  • Bach, S., Buchrieser, C., Prentice, M., Guiyoule, A., Msadek, T., Carniel, E. (1999). The High-Pathogenicity Island of Yersinia enterocolitica Ye8081 Undergoes Low-Frequency Deletion but Not Precise Excision, Suggesting Recent Stabilization in the Genome. Infect. Immun. 67: 5091-5099 [Abstract] [Full Text]  
  • Konan, K. V., Yanofsky, C. (1999). Role of Ribosome Release in Regulation of tna Operon Expression in Escherichia coli. J. Bacteriol. 181: 1530-1536 [Abstract] [Full Text]  
  • Gilsdorf, J. R. (1998). Antigenic Diversity and Gene Polymorphisms in Haemophilus influenzae. Infect. Immun. 66: 5053-5059 [Full Text]  
  • Kroll, J. S., Wilks, K. E., Farrant, J. L., Langford, P. R. (1998). Natural genetic exchange between Haemophilus and Neisseria: Intergeneric transfer of chromosomal genes between major human pathogens. Proc. Natl. Acad. Sci. USA 95: 12381-12385 [Abstract] [Full Text]  
  • Mhlanga-Mutangadura, T., Morlin, G., Smith, A. L., Eisenstark, A., Golomb, M. (1998). Evolution of the Major Pilus Gene Cluster of Haemophilus influenzae. J. Bacteriol. 180: 4693-4703 [Abstract] [Full Text]