Genome-wide analysis of ResD, NsrR, and Fur binding in Bacillus subtilis during anaerobic fermentative growth by in vivo footprinting

Onuma Chumsakul, Divya P. Anantsri, Tai Quirke, Taku Oshima, Kensuke Nakamura, Shu Ishikawa, Michiko Nakano

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Upon oxygen limitation, the Bacillus subtilis ResE sensor kinase and its cognate ResD response regulator play primary roles in the transcriptional activation of genes functioning in anaerobic respiration. The nitric oxide (NO)-sensitive NsrR repressor controls transcription to support nitrate respiration. In addition, the ferric uptake repressor (Fur) can modulate transcription under anaerobic conditions. However, whether these controls are direct or indirect has been investigated only in a gene-specific manner. To gain a genomic view of anaerobic gene regulation, we determined the genome-wide in vivo DNA binding of ResD, NsrR, and Fur transcription factors (TFs) using in situ DNase I footprinting combined with chromatin affinity precipitation sequencing (ChAP-seq; genome footprinting by high-throughput sequencing [GeF-seq]). A significant number of sites were targets of ResD and NsrR, and a majority of them were also bound by Fur. The binding of multiple TFs to overlapping targets affected each individual TF's binding, which led to combinatorial transcriptional control. ResD bound to both the promoters and the coding regions of genes under its positive control. Other genes showing enrichment of ResD at only the promoter regions are targets of direct ResD-dependent repression or antirepression. The results support previous findings of ResD as an RNA polymerase (RNAP)- binding protein and indicated that ResD can associate with the transcription elongation complex. The data set allowed us to reexamine consensus sequence motifs of Fur, ResD, and NsrR and uncovered evidence that multiple TGW (where W is A or T) sequences surrounded by an A- and T-rich sequence are often found at sites where all three TFs competitively bind.

Original languageEnglish (US)
Article numbere00086-17
JournalJournal of Bacteriology
Volume199
Issue number13
DOIs
StatePublished - Jul 1 2017

Fingerprint

Bacillus subtilis
Genome
Growth
Transcription Factors
Genes
Genetic Promoter Regions
Respiration
RNA-Binding Proteins
Deoxyribonuclease I
Consensus Sequence
DNA-Directed RNA Polymerases
Nitrates
Transcriptional Activation
Chromatin
Nitric Oxide
Phosphotransferases
Oxygen
DNA

Keywords

  • Anaerobiosis
  • Bacillus subtilis
  • Fur
  • Genome-wide binding
  • NsrR
  • ResD
  • Transcription factors

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Genome-wide analysis of ResD, NsrR, and Fur binding in Bacillus subtilis during anaerobic fermentative growth by in vivo footprinting. / Chumsakul, Onuma; Anantsri, Divya P.; Quirke, Tai; Oshima, Taku; Nakamura, Kensuke; Ishikawa, Shu; Nakano, Michiko.

In: Journal of Bacteriology, Vol. 199, No. 13, e00086-17, 01.07.2017.

Research output: Contribution to journalArticle

Chumsakul, Onuma ; Anantsri, Divya P. ; Quirke, Tai ; Oshima, Taku ; Nakamura, Kensuke ; Ishikawa, Shu ; Nakano, Michiko. / Genome-wide analysis of ResD, NsrR, and Fur binding in Bacillus subtilis during anaerobic fermentative growth by in vivo footprinting. In: Journal of Bacteriology. 2017 ; Vol. 199, No. 13.
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