Operons in Escherichia coli: genomic analyses and predictions.

The rich knowledge of operon organization in Escherichia coli, together with the completed chromosomal sequence of this bacterium, enabled us to perform an analysis of distances between genes and of functional relationships of adjacent genes in the same operon, as opposed to adjacent genes in different transcription units. We measured and demonstrated the expected tendencies of genes within operons to have much shorter intergenic distances than genes at the borders of transcription units. A clear peak at short distances between genes in the same operon contrasts with a flat frequency distribution of genes at the borders of transcription units. Also, genes in the same operon tend to have the same physiological functional class. The results of these analyses were used to implement a method to predict the genomic organization of genes into transcription units. The method has a maximum accuracy of 88% correct identification of pairs of adjacent genes to be in an operon, or at the borders of transcription units, and correctly identifies around 75% of the known transcription units when used to predict the transcription unit organization of the E. coli genome. Based on the frequency distance distributions, we estimated a total of 630 to 700 operons in E. coli. This step opens the possibility of predicting operon organization in other bacteria whose genome sequences have been finished.

[1]  J. Lawrence Selfish operons and speciation by gene transfer. , 1997, Trends in microbiology.

[2]  B. Snel,et al.  Conservation of gene order: a fingerprint of proteins that physically interact. , 1998, Trends in biochemical sciences.

[3]  F. Blattner,et al.  Functional Genomics: Expression Analysis ofEscherichia coli Growing on Minimal and Rich Media , 1999, Journal of bacteriology.

[4]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[5]  Julio Collado-Vides,et al.  RegulonDB (version 2.0): a database on transcriptional regulation in Escherichia coli , 1999, Nucleic Acids Res..

[6]  Denis Thieffry,et al.  RegulonDB: a database on transcriptional regulation in Escherichia coli , 1998, Nucleic Acids Res..

[7]  N. Glansdorff On the Origin of Operons and Their Possible Role in Evolution Toward Thermophily , 1999, Journal of Molecular Evolution.

[8]  J. Monod,et al.  Genetic regulatory mechanisms in the synthesis of proteins. , 1961, Journal of molecular biology.

[9]  M. Borodovsky,et al.  Deriving ribosomal binding site (RBS) statistical models from unannotated DNA sequences and the use of the RBS model for N-terminal prediction. , 1998, Pacific Symposium on Biocomputing. Pacific Symposium on Biocomputing.

[10]  Peter D. Karp,et al.  EcoCyc: Encyclopedia of Escherichia coli genes and metabolism , 1998, Nucleic Acids Res..

[11]  G. Sawers,et al.  Novel keto acid formate‐lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L‐threonine to propionate , 1998, Molecular microbiology.

[12]  Monica Riley,et al.  Genes and proteins of Escherichia coli K-12 , 1998, Nucleic Acids Res..

[13]  R. Overbeek,et al.  The use of gene clusters to infer functional coupling. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J R Roth,et al.  Selfish operons: horizontal transfer may drive the evolution of gene clusters. , 1996, Genetics.

[15]  J. Glasner,et al.  Genome-wide expression profiling in Escherichia coli K-12. , 1999, Nucleic acids research.

[16]  L Rychlewski,et al.  From fold predictions to function predictions: Automation of functional site conservation analysis for functional genome predictions , 1999, Protein science : a publication of the Protein Society.

[17]  Jacquelyn S. Fetrow,et al.  Functional analysis of the Escherichia coli genome for members of the α /β hydrolase family , 1998 .

[18]  Denis Thieffry,et al.  Prediction of transcriptional regulatory sites in the complete genome sequence of Escherichia coli K-12 , 1998, Bioinform..

[19]  A. Godzik,et al.  Functional insights from structural predictions: Analysis of the Escherichia coli genome , 2008, Protein science : a publication of the Protein Society.

[20]  Denis Thieffry,et al.  Syntactic recognition of regulatory regions in Escherichia coli , 1996, Comput. Appl. Biosci..

[21]  M. Riley,et al.  Functions of the gene products of Escherichia coli , 1993, Microbiological reviews.

[22]  E. Brody,et al.  Prediction of rho-independent Escherichia coli transcription terminators. A statistical analysis of their RNA stem-loop structures. , 1990 .

[23]  G. Church,et al.  A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome. , 1998, Journal of molecular biology.