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Journal of Bacteriology, September 2001, p. 5025-5040, Vol. 183, No. 17
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.17.5025-5040.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Characterizations of Highly Expressed Genes of Four
Fast-Growing Bacteria
Samuel
Karlin,1,*
Jan
Mrázek,1
Allan
Campbell,2 and
Dale
Kaiser3
Department of Mathematics, Stanford
University, Stanford, California 94305-21251;
Department of Biological Sciences, Stanford University,
Stanford, California 94305-20502; and
Department of Biochemistry, Stanford University, Stanford,
California 94305-53073
Received 25 January 2001/Accepted 7 May 2001
Predicted highly expressed (PHX) genes are characterized for the
completely sequenced genomes of the four fast-growing bacteria Escherichia coli, Haemophilus influenzae,
Vibrio cholerae, and Bacillus subtilis. Our
approach to ascertaining gene expression levels relates to
codon usage differences among certain gene classes: the collection
of all genes (average gene), the ensemble of ribosomal protein genes,
major translation/transcription processing factors, and genes for
polypeptides of chaperone/degradation complexes. A gene is predicted
highly expressed (PHX) if its codon frequencies are close to those of
the ribosomal proteins, major translation/transcription processing
factor, and chaperone/degradation standards but strongly deviant from
the average gene codon frequencies. PHX genes identified by their codon
usage frequencies among prokaryotic genomes commonly include those for
ribosomal proteins, major transcription/translation processing factors
(several occurring in multiple copies), and major chaperone/degradation
proteins. Also PHX genes generally include those encoding enzymes of
essential energy metabolism pathways of glycolysis, pyruvate oxidation,
and respiration (aerobic and anaerobic), genes of fatty acid
biosynthesis, and the principal genes of amino acid and nucleotide
biosyntheses. Gene classes generally not PHX include most repair
protein genes, virtually all vitamin biosynthesis genes, genes of
two-component sensor systems, most regulatory genes, and most genes
expressed in stationary phase or during starvation. Members of the set
of PHX aminoacyl-tRNA synthetase genes contrast sharply between
genomes. There are also subtle differences among the PHX energy
metabolism genes between E. coli and
B. subtilis, particularly with respect to genes of the tricarboxylic acid cycle. The good agreement of
PHX genes of E. coli and B. subtilis
with high protein abundances, as assessed by two-dimensional gel
determination, is verified. Relationships of PHX genes with
stoichiometry, multifunctionality, and operon structures are also
examined. The spatial distribution of PHX genes within each genome
reveals clusters and significantly long regions without PHX genes.
*
Corresponding author. Mailing address: Department of
Mathematics, Stanford University, Stanford, CA 94305-2125. Phone: (650) 723-2204. Fax: (650) 725-2040. E-mail:
karlin{at}math.stanford.edu.
Journal of Bacteriology, September 2001, p. 5025-5040, Vol. 183, No. 17
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.17.5025-5040.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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