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Title: Selection against spurious promoter motifs correlates withtranslational efficiency across bacteria

Abstract

Because binding of RNAP to misplaced sites could compromise the efficiency of transcription, natural selection for the optimization of gene expression should regulate the distribution of DNA motifs capable of RNAP-binding across the genome. Here we analyze the distribution of the -10 promoter motifs that bind the {sigma}{sup 70} subunit of RNAP in 42 bacterial genomes. We show that selection on these motifs operates across the genome, maintaining an over-representation of -10 motifs in regulatory sequences while eliminating them from the nonfunctional and, in most cases, from the protein coding regions. In some genomes, however, -10 sites are over-represented in the coding sequences; these sites could induce pauses effecting regulatory roles throughout the length of a transcriptional unit. For nonfunctional sequences, the extent of motif under-representation varies across genomes in a manner that broadly correlates with the number of tRNA genes, a good indicator of translational speed and growth rate. This suggests that minimizing the time invested in gene transcription is an important selective pressure against spurious binding. However, selection against spurious binding is detectable in the reduced genomes of host-restricted bacteria that grow at slow rates, indicating that components of efficiency other than speed may also be important. Minimizingmore » the number of RNAP molecules per cell required for transcription, and the corresponding energetic expense, may be most relevant in slow growers. These results indicate that genome-level properties affecting the efficiency of transcription and translation can respond in an integrated manner to optimize gene expression. The detection of selection against promoter motifs in nonfunctional regions also implies that no sequence may evolve free of selective constraints, at least in the relatively small and unstructured genomes of bacteria.« less

Authors:
;
Publication Date:
Research Org.:
Ernest Orlando Lawrence Berkeley NationalLaboratory, Berkeley, CA (US)
Sponsoring Org.:
USDOE Director. Office of Science. Biological andEnvironmental Research
OSTI Identifier:
929323
Report Number(s):
LBNL-63032
R&D Project: 626810; BnR: KP1103010; TRN: US200813%%187
DOE Contract Number:
DE-AC02-05CH11231
Resource Type:
Journal Article
Resource Relation:
Journal Name: Public Library of Science; Journal Volume: 2; Journal Issue: 8; Related Information: Journal Publication Date: 08/15/2007
Country of Publication:
United States
Language:
English
Subject:
59; BACTERIA; DETECTION; DISTRIBUTION; DNA; EFFICIENCY; GENES; OPTIMIZATION; PROMOTERS; PROTEINS; TRANSCRIPTION; VELOCITY

Citation Formats

Froula, Jeffrey L., and Francino, M. Pilar. Selection against spurious promoter motifs correlates withtranslational efficiency across bacteria. United States: N. p., 2007. Web.
Froula, Jeffrey L., & Francino, M. Pilar. Selection against spurious promoter motifs correlates withtranslational efficiency across bacteria. United States.
Froula, Jeffrey L., and Francino, M. Pilar. Tue . "Selection against spurious promoter motifs correlates withtranslational efficiency across bacteria". United States. doi:. https://www.osti.gov/servlets/purl/929323.
@article{osti_929323,
title = {Selection against spurious promoter motifs correlates withtranslational efficiency across bacteria},
author = {Froula, Jeffrey L. and Francino, M. Pilar},
abstractNote = {Because binding of RNAP to misplaced sites could compromise the efficiency of transcription, natural selection for the optimization of gene expression should regulate the distribution of DNA motifs capable of RNAP-binding across the genome. Here we analyze the distribution of the -10 promoter motifs that bind the {sigma}{sup 70} subunit of RNAP in 42 bacterial genomes. We show that selection on these motifs operates across the genome, maintaining an over-representation of -10 motifs in regulatory sequences while eliminating them from the nonfunctional and, in most cases, from the protein coding regions. In some genomes, however, -10 sites are over-represented in the coding sequences; these sites could induce pauses effecting regulatory roles throughout the length of a transcriptional unit. For nonfunctional sequences, the extent of motif under-representation varies across genomes in a manner that broadly correlates with the number of tRNA genes, a good indicator of translational speed and growth rate. This suggests that minimizing the time invested in gene transcription is an important selective pressure against spurious binding. However, selection against spurious binding is detectable in the reduced genomes of host-restricted bacteria that grow at slow rates, indicating that components of efficiency other than speed may also be important. Minimizing the number of RNAP molecules per cell required for transcription, and the corresponding energetic expense, may be most relevant in slow growers. These results indicate that genome-level properties affecting the efficiency of transcription and translation can respond in an integrated manner to optimize gene expression. The detection of selection against promoter motifs in nonfunctional regions also implies that no sequence may evolve free of selective constraints, at least in the relatively small and unstructured genomes of bacteria.},
doi = {},
journal = {Public Library of Science},
number = 8,
volume = 2,
place = {United States},
year = {Tue May 01 00:00:00 EDT 2007},
month = {Tue May 01 00:00:00 EDT 2007}
}