Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12

The identification of regulatory targets of all transcription factors (TFs) is critical for understanding the entire network of genome regulation. A total of approximately 300 TFs exist in the model prokaryote Escherichia coli K-12, but the identification of whole sets of their direct targets is imp...

Full description

Bibliographic Details
Main Authors: Tomohiro Shimada, Hiroshi Ogasawara, Ikki Kobayashi, Naoki Kobayashi, Akira Ishihama
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.697803/full
_version_ 1819045320473968640
author Tomohiro Shimada
Hiroshi Ogasawara
Hiroshi Ogasawara
Ikki Kobayashi
Naoki Kobayashi
Akira Ishihama
Akira Ishihama
author_facet Tomohiro Shimada
Hiroshi Ogasawara
Hiroshi Ogasawara
Ikki Kobayashi
Naoki Kobayashi
Akira Ishihama
Akira Ishihama
author_sort Tomohiro Shimada
collection DOAJ
description The identification of regulatory targets of all transcription factors (TFs) is critical for understanding the entire network of genome regulation. A total of approximately 300 TFs exist in the model prokaryote Escherichia coli K-12, but the identification of whole sets of their direct targets is impossible with use of in vivo approaches. For this end, the most direct and quick approach is to identify the TF-binding sites in vitro on the genome. We then developed and utilized the gSELEX screening system in vitro for identification of more than 150 E. coli TF-binding sites along the E. coli genome. Based on the number of predicted regulatory targets, we classified E. coli K-12 TFs into four groups, altogether forming a hierarchy ranging from a single-target TF (ST-TF) to local TFs, global TFs, and nucleoid-associated TFs controlling as many as 1,000 targets. Using the collection of purified TFs and a library of genome DNA segments from a single and the same E. coli K-12, we identified here a total of 11 novel ST-TFs, CsqR, CusR, HprR, NorR, PepA, PutA, QseA, RspR, UvrY, ZraR, and YqhC. The regulation of single-target promoters was analyzed in details for the hitherto uncharacterized QseA and RspR. In most cases, the ST-TF gene and its regulatory target genes are adjacently located on the E. coli K-12 genome, implying their simultaneous transfer in the course of genome evolution. The newly identified 11 ST-TFs and the total of 13 hitherto identified altogether constitute the minority group of TFs in E. coli K-12.
first_indexed 2024-12-21T10:26:42Z
format Article
id doaj.art-1e51e31cd3f64448b304a2650f0aa8ba
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-21T10:26:42Z
publishDate 2021-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-1e51e31cd3f64448b304a2650f0aa8ba2022-12-21T19:07:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-06-011210.3389/fmicb.2021.697803697803Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12Tomohiro Shimada0Hiroshi Ogasawara1Hiroshi Ogasawara2Ikki Kobayashi3Naoki Kobayashi4Akira Ishihama5Akira Ishihama6School of Agriculture, Meiji University, Kawasaki, JapanResearch Center for Supports to Advanced Science, Division of Gene Research, Shinshu University, Nagano, JapanResearch Center for Fungal and Microbial Dynamism, Shinshu University, Nagano, JapanSchool of Agriculture, Meiji University, Kawasaki, JapanDepartment of Frontier Science, Hosei University, Koganei, JapanDepartment of Frontier Science, Hosei University, Koganei, JapanMicro-Nano Technology Research Center, Hosei University, Koganei, JapanThe identification of regulatory targets of all transcription factors (TFs) is critical for understanding the entire network of genome regulation. A total of approximately 300 TFs exist in the model prokaryote Escherichia coli K-12, but the identification of whole sets of their direct targets is impossible with use of in vivo approaches. For this end, the most direct and quick approach is to identify the TF-binding sites in vitro on the genome. We then developed and utilized the gSELEX screening system in vitro for identification of more than 150 E. coli TF-binding sites along the E. coli genome. Based on the number of predicted regulatory targets, we classified E. coli K-12 TFs into four groups, altogether forming a hierarchy ranging from a single-target TF (ST-TF) to local TFs, global TFs, and nucleoid-associated TFs controlling as many as 1,000 targets. Using the collection of purified TFs and a library of genome DNA segments from a single and the same E. coli K-12, we identified here a total of 11 novel ST-TFs, CsqR, CusR, HprR, NorR, PepA, PutA, QseA, RspR, UvrY, ZraR, and YqhC. The regulation of single-target promoters was analyzed in details for the hitherto uncharacterized QseA and RspR. In most cases, the ST-TF gene and its regulatory target genes are adjacently located on the E. coli K-12 genome, implying their simultaneous transfer in the course of genome evolution. The newly identified 11 ST-TFs and the total of 13 hitherto identified altogether constitute the minority group of TFs in E. coli K-12.https://www.frontiersin.org/articles/10.3389/fmicb.2021.697803/fulltranscription regulatorsingle-target transcription factorgenomic SELEXEscherichia coli K-12QseARspR
spellingShingle Tomohiro Shimada
Hiroshi Ogasawara
Hiroshi Ogasawara
Ikki Kobayashi
Naoki Kobayashi
Akira Ishihama
Akira Ishihama
Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12
Frontiers in Microbiology
transcription regulator
single-target transcription factor
genomic SELEX
Escherichia coli K-12
QseA
RspR
title Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12
title_full Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12
title_fullStr Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12
title_full_unstemmed Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12
title_short Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12
title_sort single target regulators constitute the minority group of transcription factors in escherichia coli k 12
topic transcription regulator
single-target transcription factor
genomic SELEX
Escherichia coli K-12
QseA
RspR
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.697803/full
work_keys_str_mv AT tomohiroshimada singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12
AT hiroshiogasawara singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12
AT hiroshiogasawara singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12
AT ikkikobayashi singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12
AT naokikobayashi singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12
AT akiraishihama singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12
AT akiraishihama singletargetregulatorsconstitutetheminoritygroupoftranscriptionfactorsinescherichiacolik12