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Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa

Much of our knowledge of bacterial transcription initiation has been derived from studying the promoters of Escherichia coli and Bacillus subtilis. Given the expansive diversity across the bacterial phylogeny, it is unclear how much of this knowledge can be applied to other organisms. Here, we repor...

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Autores principales: Myers, Kevin S., Noguera, Daniel R., Donohue, Timothy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8407463/
https://www.ncbi.nlm.nih.gov/pubmed/34254822
http://dx.doi.org/10.1128/mSystems.00526-21
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author Myers, Kevin S.
Noguera, Daniel R.
Donohue, Timothy J.
author_facet Myers, Kevin S.
Noguera, Daniel R.
Donohue, Timothy J.
author_sort Myers, Kevin S.
collection PubMed
description Much of our knowledge of bacterial transcription initiation has been derived from studying the promoters of Escherichia coli and Bacillus subtilis. Given the expansive diversity across the bacterial phylogeny, it is unclear how much of this knowledge can be applied to other organisms. Here, we report on bioinformatic analyses of promoter sequences of the primary σ factor (σ(70)) by leveraging publicly available transcription start site (TSS) sequencing data sets for nine bacterial species spanning five phyla. This analysis identifies previously unreported differences in the −35 and −10 elements of σ(70)-dependent promoters in several groups of bacteria. We found that Actinobacteria and Betaproteobacteria σ(70)-dependent promoters lack the TTG triad in their −35 element, which is predicted to be conserved across the bacterial phyla. In addition, the majority of the Alphaproteobacteria σ(70)-dependent promoters analyzed lacked the thymine at position −7 that is highly conserved in other phyla. Bioinformatic examination of the Alphaproteobacteria σ(70)-dependent promoters identifies a significant overrepresentation of essential genes and ones encoding proteins with common cellular functions downstream of promoters containing an A, C, or G at position −7. We propose that transcription of many σ(70)-dependent promoters in Alphaproteobacteria depends on the transcription factor CarD, which is an essential protein in several members of this phylum. Our analysis expands the knowledge of promoter architecture across the bacterial phylogeny and provides new information that can be used to engineer bacteria for use in medical, environmental, agricultural, and biotechnological processes. IMPORTANCE Transcription of DNA to RNA by RNA polymerase is essential for cells to grow, develop, and respond to stress. Understanding the process and control of transcription is important for health, disease, the environment, and biotechnology. Decades of research on a few bacteria have identified promoter DNA sequences that are recognized by the σ subunit of RNA polymerase. We used bioinformatic analyses to reveal previously unreported differences in promoter DNA sequences across the bacterial phylogeny. We found that many Actinobacteria and Betaproteobacteria promoters lack a sequence in their −35 DNA recognition element that was previously assumed to be conserved and that Alphaproteobacteria lack a thymine residue at position −7, also previously assumed to be conserved. Our work reports important new information about bacterial transcription, illustrates the benefits of studying bacteria across the phylogenetic tree, and proposes new lines of future investigation.
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spelling pubmed-84074632021-09-09 Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa Myers, Kevin S. Noguera, Daniel R. Donohue, Timothy J. mSystems Research Article Much of our knowledge of bacterial transcription initiation has been derived from studying the promoters of Escherichia coli and Bacillus subtilis. Given the expansive diversity across the bacterial phylogeny, it is unclear how much of this knowledge can be applied to other organisms. Here, we report on bioinformatic analyses of promoter sequences of the primary σ factor (σ(70)) by leveraging publicly available transcription start site (TSS) sequencing data sets for nine bacterial species spanning five phyla. This analysis identifies previously unreported differences in the −35 and −10 elements of σ(70)-dependent promoters in several groups of bacteria. We found that Actinobacteria and Betaproteobacteria σ(70)-dependent promoters lack the TTG triad in their −35 element, which is predicted to be conserved across the bacterial phyla. In addition, the majority of the Alphaproteobacteria σ(70)-dependent promoters analyzed lacked the thymine at position −7 that is highly conserved in other phyla. Bioinformatic examination of the Alphaproteobacteria σ(70)-dependent promoters identifies a significant overrepresentation of essential genes and ones encoding proteins with common cellular functions downstream of promoters containing an A, C, or G at position −7. We propose that transcription of many σ(70)-dependent promoters in Alphaproteobacteria depends on the transcription factor CarD, which is an essential protein in several members of this phylum. Our analysis expands the knowledge of promoter architecture across the bacterial phylogeny and provides new information that can be used to engineer bacteria for use in medical, environmental, agricultural, and biotechnological processes. IMPORTANCE Transcription of DNA to RNA by RNA polymerase is essential for cells to grow, develop, and respond to stress. Understanding the process and control of transcription is important for health, disease, the environment, and biotechnology. Decades of research on a few bacteria have identified promoter DNA sequences that are recognized by the σ subunit of RNA polymerase. We used bioinformatic analyses to reveal previously unreported differences in promoter DNA sequences across the bacterial phylogeny. We found that many Actinobacteria and Betaproteobacteria promoters lack a sequence in their −35 DNA recognition element that was previously assumed to be conserved and that Alphaproteobacteria lack a thymine residue at position −7, also previously assumed to be conserved. Our work reports important new information about bacterial transcription, illustrates the benefits of studying bacteria across the phylogenetic tree, and proposes new lines of future investigation. American Society for Microbiology 2021-07-13 /pmc/articles/PMC8407463/ /pubmed/34254822 http://dx.doi.org/10.1128/mSystems.00526-21 Text en Copyright © 2021 Myers et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Myers, Kevin S.
Noguera, Daniel R.
Donohue, Timothy J.
Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa
title Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa
title_full Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa
title_fullStr Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa
title_full_unstemmed Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa
title_short Promoter Architecture Differences among Alphaproteobacteria and Other Bacterial Taxa
title_sort promoter architecture differences among alphaproteobacteria and other bacterial taxa
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8407463/
https://www.ncbi.nlm.nih.gov/pubmed/34254822
http://dx.doi.org/10.1128/mSystems.00526-21
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