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
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
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 Xie, G.
Right arrow Articles by Jensen, R. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Xie, G.
Right arrow Articles by Jensen, R. A.

Next Article 

Microbiology and Molecular Biology Reviews, September 2003, p. 303-342, Vol. 67, No. 3
1092-2172/03/$08.00+0     DOI: 10.1128/MMBR.67.3.303-342.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Ancient Origin of the Tryptophan Operon and the Dynamics of Evolutionary Change{dagger}

Gary Xie,1,2 Nemat O. Keyhani,1* Carol A. Bonner,1 and Roy A. Jensen1,2,3*

Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida 32611,1 BioScience Division, Los Alamos National Laboratory, Los Alamos, New Mexico 87544,2 Department of Chemistry, City College of New York, New York, New York 100313

The seven conserved enzymatic domains required for tryptophan (Trp) biosynthesis are encoded in seven genetic regions that are organized differently (whole-pathway operons, multiple partial-pathway operons, and dispersed genes) in prokaryotes. A comparative bioinformatics evaluation of the conservation and organization of the genes of Trp biosynthesis in prokaryotic operons should serve as an excellent model for assessing the feasibility of predicting the evolutionary histories of genes and operons associated with other biochemical pathways. These comparisons should provide a better understanding of possible explanations for differences in operon organization in different organisms at a genomics level. These analyses may also permit identification of some of the prevailing forces that dictated specific gene rearrangements during the course of evolution. Operons concerned with Trp biosynthesis in prokaryotes have been in a dynamic state of flux. Analysis of closely related organisms among the Bacteria at various phylogenetic nodes reveals many examples of operon scission, gene dispersal, gene fusion, gene scrambling, and gene loss from which the direction of evolutionary events can be deduced. Two milestone evolutionary events have been mapped to the 16S rRNA tree of Bacteria, one splitting the operon in two, and the other rejoining it by gene fusion. The Archaea, though less resolved due to a lesser genome representation, appear to exhibit more gene scrambling than the Bacteria. The trp operon appears to have been an ancient innovation; it was already present in the common ancestor of Bacteria and Archaea. Although the operon has been subjected, even in recent times, to dynamic changes in gene rearrangement, the ancestral gene order can be deduced with confidence. The evolutionary history of the genes of the pathway is discernible in rough outline as a vertical line of descent, with events of lateral gene transfer or paralogy enriching the analysis as interesting features that can be distinguished. As additional genomes are thoroughly analyzed, an increasingly refined resolution of the sequential evolutionary steps is clearly possible. These comparisons suggest that present-day trp operons that possess finely tuned regulatory features are under strong positive selection and are able to resist the disruptive evolutionary events that may be experienced by simpler, poorly regulated operons.

* Corresponding author. Mailing address: Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611. Fax: (352) 392-5922. Phone for Nemat Keyhani: (352) 392-2488. E-mail: nkeyhani{at}ufl.edu. Phone for Roy Jensen: (352) 475-3019. E-mail: rjensen{at}ufl.edu.

{dagger} Florida Agricultural Experiment Station Journal series no. R-09160.

Microbiology and Molecular Biology Reviews, September 2003, p. 303-342, Vol. 67, No. 3
1092-2172/03/$08.00+0     DOI: 10.1128/MMBR.67.3.303-342.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Lo, C.-C., Bonner, C. A., Xie, G., D'Souza, M., Jensen, R. A. (2009). Cohesion Group Approach for Evolutionary Analysis of Aspartokinase, an Enzyme That Feeds a Branched Network of Many Biochemical Pathways. Microbiol. Mol. Biol. Rev. 73: 594-651 [Abstract] [Full Text]  
  • Sorrels, C. M., Proteau, P. J., Gerwick, W. H. (2009). Organization, Evolution, and Expression Analysis of the Biosynthetic Gene Cluster for Scytonemin, a Cyanobacterial UV-Absorbing Pigment. Appl. Environ. Microbiol. 75: 4861-4869 [Abstract] [Full Text]  
  • Whitman, W. B. (2009). The Modern Concept of the Procaryote. J. Bacteriol. 191: 2000-2005 [Full Text]  
  • Karr, E. A., Sandman, K., Lurz, R., Reeve, J. N. (2008). TrpY Regulation of trpB2 Transcription in Methanothermobacter thermautotrophicus. J. Bacteriol. 190: 2637-2641 [Abstract] [Full Text]  
  • Bonner, C. A., Disz, T., Hwang, K., Song, J., Vonstein, V., Overbeek, R., Jensen, R. A. (2008). Cohesion Group Approach for Evolutionary Analysis of TyrA, a Protein Family with Wide-Ranging Substrate Specificities. Microbiol. Mol. Biol. Rev. 72: 13-53 [Abstract] [Full Text]  
  • Cubonova, L., Sandman, K., Karr, E. A., Cochran, A. J., Reeve, J. N. (2007). Spontaneous trpY Mutants and Mutational Analysis of the TrpY Archaeal Transcription Regulator. J. Bacteriol. 189: 4338-4342 [Abstract] [Full Text]  
  • Moran, N. A. (2007). Colloquium Papers: Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl. Acad. Sci. USA 104: 8627-8633 [Abstract] [Full Text]  
  • Nakamura, Y., Itoh, T., Martin, W. (2007). Rate and Polarity of Gene Fusion and Fission in Oryza sativa and Arabidopsis thaliana. Mol Biol Evol 24: 110-121 [Abstract] [Full Text]  
  • Klotz, M. G., Arp, D. J., Chain, P. S. G., El-Sheikh, A. F., Hauser, L. J., Hommes, N. G., Larimer, F. W., Malfatti, S. A., Norton, J. M., Poret-Peterson, A. T., Vergez, L. M., Ward, B. B. (2006). Complete Genome Sequence of the Marine, Chemolithoautotrophic, Ammonia-Oxidizing Bacterium Nitrosococcus oceani ATCC 19707. Appl. Environ. Microbiol. 72: 6299-6315 [Abstract] [Full Text]  
  • Overbeek, R., Begley, T., Butler, R. M., Choudhuri, J. V., Chuang, H.-Y., Cohoon, M., de Crecy-Lagard, V., Diaz, N., Disz, T., Edwards, R., Fonstein, M., Frank, E. D., Gerdes, S., Glass, E. M., Goesmann, A., Hanson, A., Iwata-Reuyl, D., Jensen, R., Jamshidi, N., Krause, L., Kubal, M., Larsen, N., Linke, B., McHardy, A. C., Meyer, F., Neuweger, H., Olsen, G., Olson, R., Osterman, A., Portnoy, V., Pusch, G. D., Rodionov, D. A., Ruckert, C., Steiner, J., Stevens, R., Thiele, I., Vassieva, O., Ye, Y., Zagnitko, O., Vonstein, V. (2005). The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes. Nucleic Acids Res 33: 5691-5702 [Abstract] [Full Text]  
  • Xie, Y., Reeve, J. N. (2005). Regulation of Tryptophan Operon Expression in the Archaeon Methanothermobacter thermautotrophicus. J. Bacteriol. 187: 6419-6429 [Abstract] [Full Text]  
  • Porat, I., Waters, B. W., Teng, Q., Whitman, W. B. (2004). Two Biosynthetic Pathways for Aromatic Amino Acids in the Archaeon Methanococcus maripaludis. J. Bacteriol. 186: 4940-4950 [Abstract] [Full Text]  


Copyright © 2010 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»