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Mix-and-matching as a promoter recognition mechanism by ECF σ factors

BACKGROUND: Transcription initiation is in bacteria exhibited by different σ factors, most of which fall within σ(70) family. This family is diverse, ranging from the housekeeping Group I (RpoDs), to Group IV (ECF) σ factors, that transcribe smaller regulons under more stringent conditions. RpoDs em...

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Autores principales: Guzina, Jelena, Djordjevic, Marko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5333181/
https://www.ncbi.nlm.nih.gov/pubmed/28251873
http://dx.doi.org/10.1186/s12862-016-0865-z
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author Guzina, Jelena
Djordjevic, Marko
author_facet Guzina, Jelena
Djordjevic, Marko
author_sort Guzina, Jelena
collection PubMed
description BACKGROUND: Transcription initiation is in bacteria exhibited by different σ factors, most of which fall within σ(70) family. This family is diverse, ranging from the housekeeping Group I (RpoDs), to Group IV (ECF) σ factors, that transcribe smaller regulons under more stringent conditions. RpoDs employ a kinetic mix-and-match mechanism, where promoter elements complement each other binding strengths in achieving sufficient transcription activity. On the other hand, it is assumed that ECF σs, which are the most distant from the housekeeping σ factors, cannot exhibit mix-and-matching. However, mix-and-matching for ECF σ factors was not quantitatively checked before, and recent results show a much larger flexibility in the promoter recognition by the members of this group. RESULTS: To this end, we quantitatively investigate mix-and-matching in two canonical ECF σ family members (σ(E) and σ(W)), for which we use a biophysics based model of transcription initiation. For σ(E), we perform a separate analysis for in-vitro active and in-vitro inactive promoters, which allows us investigating how mix-and-matching depends on the external factors that may control transcription activity in the in-vitro inactive set. We show that the promoter elements of canonical ECF σs significantly complement each other strengths, where such mix-and-matching is in the in-vitro active set even stronger compared to the correlations observed for the housekeeping σs. This complementation however significantly decreases for the in-vitro inactive set, which we propose is due to mix-and-matching with regulatory sequences outside of the canonical promoter elements. In line with this proposition, we show that a conserved spacer element, which appears in the in-vitro inactive promoter set, significantly increases the promoter element complementation. While RpoD promoter elements mix-and-match to achieve sufficient total transcription activity, for σ(E) they complement each other to achieve sufficiently strong total binding affinity, which we relate to differences in physiological responses between the two groups of σ factors. CONCLUSION: Despite a common notion that smaller σ factor specificity leads to a larger mix-and-matching, we here obtain a larger promoter element complementation for σ(E) compared to RpoDs. Finally, to explain this finding, we propose a simple model which relates the size of σ factor regulon with the extent of mix-and-matching, based on an assumption of a selection pressure on promoters that are near the non-specific binding boundary to remain functional. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0865-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-53331812017-03-06 Mix-and-matching as a promoter recognition mechanism by ECF σ factors Guzina, Jelena Djordjevic, Marko BMC Evol Biol Research BACKGROUND: Transcription initiation is in bacteria exhibited by different σ factors, most of which fall within σ(70) family. This family is diverse, ranging from the housekeeping Group I (RpoDs), to Group IV (ECF) σ factors, that transcribe smaller regulons under more stringent conditions. RpoDs employ a kinetic mix-and-match mechanism, where promoter elements complement each other binding strengths in achieving sufficient transcription activity. On the other hand, it is assumed that ECF σs, which are the most distant from the housekeeping σ factors, cannot exhibit mix-and-matching. However, mix-and-matching for ECF σ factors was not quantitatively checked before, and recent results show a much larger flexibility in the promoter recognition by the members of this group. RESULTS: To this end, we quantitatively investigate mix-and-matching in two canonical ECF σ family members (σ(E) and σ(W)), for which we use a biophysics based model of transcription initiation. For σ(E), we perform a separate analysis for in-vitro active and in-vitro inactive promoters, which allows us investigating how mix-and-matching depends on the external factors that may control transcription activity in the in-vitro inactive set. We show that the promoter elements of canonical ECF σs significantly complement each other strengths, where such mix-and-matching is in the in-vitro active set even stronger compared to the correlations observed for the housekeeping σs. This complementation however significantly decreases for the in-vitro inactive set, which we propose is due to mix-and-matching with regulatory sequences outside of the canonical promoter elements. In line with this proposition, we show that a conserved spacer element, which appears in the in-vitro inactive promoter set, significantly increases the promoter element complementation. While RpoD promoter elements mix-and-match to achieve sufficient total transcription activity, for σ(E) they complement each other to achieve sufficiently strong total binding affinity, which we relate to differences in physiological responses between the two groups of σ factors. CONCLUSION: Despite a common notion that smaller σ factor specificity leads to a larger mix-and-matching, we here obtain a larger promoter element complementation for σ(E) compared to RpoDs. Finally, to explain this finding, we propose a simple model which relates the size of σ factor regulon with the extent of mix-and-matching, based on an assumption of a selection pressure on promoters that are near the non-specific binding boundary to remain functional. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0865-z) contains supplementary material, which is available to authorized users. BioMed Central 2017-02-07 /pmc/articles/PMC5333181/ /pubmed/28251873 http://dx.doi.org/10.1186/s12862-016-0865-z Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Guzina, Jelena
Djordjevic, Marko
Mix-and-matching as a promoter recognition mechanism by ECF σ factors
title Mix-and-matching as a promoter recognition mechanism by ECF σ factors
title_full Mix-and-matching as a promoter recognition mechanism by ECF σ factors
title_fullStr Mix-and-matching as a promoter recognition mechanism by ECF σ factors
title_full_unstemmed Mix-and-matching as a promoter recognition mechanism by ECF σ factors
title_short Mix-and-matching as a promoter recognition mechanism by ECF σ factors
title_sort mix-and-matching as a promoter recognition mechanism by ecf σ factors
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5333181/
https://www.ncbi.nlm.nih.gov/pubmed/28251873
http://dx.doi.org/10.1186/s12862-016-0865-z
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