ArticlePLoS biology2009
Stochasticity in protein levels drives colinearity of gene order in metabolic operons of Escherichia coli.
Article in PLoS biology, 2009. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 21 papers.
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Who cites it
21 citing papers in PubMed.
- Article
- The Exploration of Novel Regulatory Relationships Drives Haloarchaeal Operon-Like Structural Dynamics over Short Evolutionary Distances.Microorganisms · 2020Article
- Investigation on the Evolutionary Relation of Diverse Polyhydroxyalkanoate Gene Clusters in Betaproteobacteria.Journal of molecular evolution · 2018Article
- Cellular Growth Arrest and Persistence from Enzyme Saturation.PLoS computational biology · 2016Article
- Operon Gene Order Is Optimized for Ordered Protein Complex Assembly.Cell reports · 2016Article
- Coevolution of the Organization and Structure of Prokaryotic Genomes.Cold Spring Harbor perspectives in biology · 2016Review
- Bacterial protein networks: properties and functions.Nature reviews. Microbiology · 2015Review
- Natural selection for operons depends on genome size.Genome biology and evolution · 2013Article
- Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca.Proceedings of the National Academy of Sciences of the United States of America · 2012Article
- Validation of the essential ClpP protease in Mycobacterium tuberculosis as a novel drug target.Journal of bacteriology · 2012Article
- A genome-wide analysis of promoter-mediated phenotypic noise in Escherichia coli.PLoS genetics · 2012Article
- Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.PLoS computational biology · 2012Article
- Error prevention and mitigation as forces in the evolution of genes and genomes.Nature reviews. Genetics · 2011Review
- Fundamental relationship between operon organization and gene expression.Proceedings of the National Academy of Sciences of the United States of America · 2011Article
- Impact of gene expression noise on organismal fitness and the efficacy of natural selection.Proceedings of the National Academy of Sciences of the United States of America · 2011Article
- The pseudogenes of Mycobacterium leprae reveal the functional relevance of gene order within operons.Nucleic acids research · 2011Article
- Transcriptional coupling of neighboring genes and gene expression noise: evidence that gene orientation and noncoding transcripts are modulators of noise.Genome biology and evolution · 2011Article
- Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation.The Journal of biological chemistry · 2010Article
- Selection upon genome architecture: conservation of functional neighborhoods with changing genes.PLoS computational biology · 2010Article
- Messy biology and the origins of evolutionary innovations.Nature chemical biology · 2010Article
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Authors and funding
3 authors.
Funding
No grant is acknowledged in the PubMed record.
Abstract
In bacterial genomes, gene order is not random. This is most evident when looking at operons, these often encoding enzymes involved in the same metabolic pathway or proteins from the same complex. Is gene order within operons nonrandom, however, and if so why? We examine this issue using metabolic operons as a case study. Using the metabolic network of Escherichia coli, we define the temporal order of reactions. We find a pronounced trend for genes to appear in operons in the same order as they are needed in metabolism (colinearity). This is paradoxical as, at steady state, enzymes abundance should be independent of order within the operon. We consider three extensions of the steady-state model that could potentially account for colinearity: (1) increased productivity associated with higher expression levels of the most 5' genes, (2) a faster metabolic processing immediately after up-regulation, and (3) metabolic stalling owing to stochastic protein loss. We establish the validity of these hypotheses by employing deterministic and stochastic models of enzyme kinetics. The stochastic stalling hypothesis correctly and uniquely predicts that colinearity is more pronounced both for lowly expressed operons and for genes that are not physically adjacent. The alternative models fail to find any support. These results support the view that stochasticity is a pervasive problem to a cell and that gene order evolution can be driven by the selective consequences of fluctuations in protein levels.
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