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Title: The Life-cycle of Operons

Abstract

Operons are a major feature of all prokaryotic genomes, but how and why operon structures vary is not well understood. To elucidate the life-cycle of operons, we compared gene order between Escherichia coli K12 and its relatives and identified the recently formed and destroyed operons in E. coli. This allowed us to determine how operons form, how they become closely spaced, and how they die. Our findings suggest that operon evolution is driven by selection on gene expression patterns. First, both operon creation and operon destruction lead to large changes in gene expression patterns. For example, the removal of lysA and ruvA from ancestral operons that contained essential genes allowed their expression to respond to lysine levels and DNA damage, respectively. Second, some operons have undergone accelerated evolution, with multiple new genes being added during a brief period. Third, although most operons are closely spaced because of a neutral bias towards deletion and because of selection against large overlaps, highly expressed operons tend to be widely spaced because of regulatory fine-tuning by intervening sequences. Although operon evolution seems to be adaptive, it need not be optimal: new operons often comprise functionally unrelated genes that were already in proximity before themore » operon formed.« less

Authors:
; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Director. Office of Science. Office of Biological andEnvironmental Research, Genomics:GTL Program; Howard Hughes MedicalInstitute
OSTI Identifier:
889264
Report Number(s):
LBNL-61256
R&D Project: VGTLAA; BnR: KP1102010; TRN: US200623%%759
DOE Contract Number:  
DE-AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 2; Journal Issue: 7; Related Information: Journal Publication Date: 07/28/2006
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 42 ENGINEERING; DNA DAMAGES; ESCHERICHIA COLI; GENES; LIFE CYCLE; LYSINE; REMOVAL; Operon genome life-cycle gene expression

Citation Formats

Price, Morgan N, Arkin, Adam P, and Alm, Eric J. The Life-cycle of Operons. United States: N. p., 2005. Web.
Price, Morgan N, Arkin, Adam P, & Alm, Eric J. The Life-cycle of Operons. United States.
Price, Morgan N, Arkin, Adam P, and Alm, Eric J. 2005. "The Life-cycle of Operons". United States. https://www.osti.gov/servlets/purl/889264.
@article{osti_889264,
title = {The Life-cycle of Operons},
author = {Price, Morgan N and Arkin, Adam P and Alm, Eric J},
abstractNote = {Operons are a major feature of all prokaryotic genomes, but how and why operon structures vary is not well understood. To elucidate the life-cycle of operons, we compared gene order between Escherichia coli K12 and its relatives and identified the recently formed and destroyed operons in E. coli. This allowed us to determine how operons form, how they become closely spaced, and how they die. Our findings suggest that operon evolution is driven by selection on gene expression patterns. First, both operon creation and operon destruction lead to large changes in gene expression patterns. For example, the removal of lysA and ruvA from ancestral operons that contained essential genes allowed their expression to respond to lysine levels and DNA damage, respectively. Second, some operons have undergone accelerated evolution, with multiple new genes being added during a brief period. Third, although most operons are closely spaced because of a neutral bias towards deletion and because of selection against large overlaps, highly expressed operons tend to be widely spaced because of regulatory fine-tuning by intervening sequences. Although operon evolution seems to be adaptive, it need not be optimal: new operons often comprise functionally unrelated genes that were already in proximity before the operon formed.},
doi = {},
url = {https://www.osti.gov/biblio/889264}, journal = {PLoS Genetics},
number = 7,
volume = 2,
place = {United States},
year = {Fri Nov 18 00:00:00 EST 2005},
month = {Fri Nov 18 00:00:00 EST 2005}
}