Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.

Bacterial chromosomes are organized into polycistronic cotranscribed operons, but the evolutionary pressures maintaining them are unclear. We hypothesized that operons alter gene expression noise characteristics, resulting in selection for or against maintaining operons depending on network architec...

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Autores principales: J Christian J Ray, Oleg A Igoshin
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Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/2aea96f88df34d66a1a4cf130f055dca
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spelling oai:doaj.org-article:2aea96f88df34d66a1a4cf130f055dca2021-11-18T05:51:01ZInterplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.1553-734X1553-735810.1371/journal.pcbi.1002672https://doaj.org/article/2aea96f88df34d66a1a4cf130f055dca2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22956903/pdf/?tool=EBIhttps://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Bacterial chromosomes are organized into polycistronic cotranscribed operons, but the evolutionary pressures maintaining them are unclear. We hypothesized that operons alter gene expression noise characteristics, resulting in selection for or against maintaining operons depending on network architecture. Mathematical models for 6 functional classes of network modules showed that three classes exhibited decreased noise and 3 exhibited increased noise with same-operon cotranscription of interacting proteins. Noise reduction was often associated with a decreased chance of reaching an ultrasensitive threshold. Stochastic simulations of the lac operon demonstrated that the predicted effects of transcriptional coupling hold for a complex network module. We employed bioinformatic analysis to find overrepresentation of noise-minimizing operon organization compared with randomized controls. Among constitutively expressed physically interacting protein pairs, higher coupling frequencies appeared at lower expression levels, where noise effects are expected to be dominant. Our results thereby suggest an important role for gene expression noise, in many cases interacting with an ultrasensitive switch, in maintaining or selecting for operons in bacterial chromosomes.J Christian J RayOleg A IgoshinPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 8, Iss 8, p e1002672 (2012)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
J Christian J Ray
Oleg A Igoshin
Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
description Bacterial chromosomes are organized into polycistronic cotranscribed operons, but the evolutionary pressures maintaining them are unclear. We hypothesized that operons alter gene expression noise characteristics, resulting in selection for or against maintaining operons depending on network architecture. Mathematical models for 6 functional classes of network modules showed that three classes exhibited decreased noise and 3 exhibited increased noise with same-operon cotranscription of interacting proteins. Noise reduction was often associated with a decreased chance of reaching an ultrasensitive threshold. Stochastic simulations of the lac operon demonstrated that the predicted effects of transcriptional coupling hold for a complex network module. We employed bioinformatic analysis to find overrepresentation of noise-minimizing operon organization compared with randomized controls. Among constitutively expressed physically interacting protein pairs, higher coupling frequencies appeared at lower expression levels, where noise effects are expected to be dominant. Our results thereby suggest an important role for gene expression noise, in many cases interacting with an ultrasensitive switch, in maintaining or selecting for operons in bacterial chromosomes.
format article
author J Christian J Ray
Oleg A Igoshin
author_facet J Christian J Ray
Oleg A Igoshin
author_sort J Christian J Ray
title Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
title_short Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
title_full Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
title_fullStr Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
title_full_unstemmed Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
title_sort interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/2aea96f88df34d66a1a4cf130f055dca
work_keys_str_mv AT jchristianjray interplayofgeneexpressionnoiseandultrasensitivedynamicsaffectsbacterialoperonorganization
AT olegaigoshin interplayofgeneexpressionnoiseandultrasensitivedynamicsaffectsbacterialoperonorganization
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