A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth

Constantinidou, Chrystala; Hobman, Jon L.; Griffiths, Lesley; Patel, Mala D.; Penn, Charles W.; Cole, Jeffrey A.; Overton, Tim W.

doi:10.1074/jbc.m512312200

Cited by 280Bacterial Genetics and BiotechnologyEscherichia coli research studiesMicrobial Metabolic Engineering and Bioproduction

A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth

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Constantinidou, Chrystala, Hobman, Jon L., Griffiths, Lesley, Patel, Mala D., Penn, Charles W., Cole, Jeffrey A., Overton, Tim W.·2006·Journal of Biological Chemistry

DOI 10.1074/jbc.m512312200

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Abstract

The transcription factor FNR, the regulator of fumarate and nitrate reduction, regulates major changes as Escherichia coli adapts from aerobic to anaerobic growth. In an anaerobic glycerol/trimethylamine N-oxide/fumarate medium, the fnr mutant grew as well as the parental strain, E. coli K12 MG1655, enabling us to reveal the response to oxygen, nitrate, and nitrite in the absence of glucose repression or artifacts because of variations in growth rate. Hence, many of the discrepancies between previous microarray studies of the E. coli FNR regulon were resolved. The current microarray data confirmed 31 of the previously characterized FNR-regulated operons. Forty four operons not previously known to be included in the FNR regulon were activated by FNR, and a further 28 operons appeared to be repressed. For each of these operons, a match to the consensus FNR-binding site sequence was identified. The FNR regulon therefore minimally includes at least 103, and possibly as many as 115, operons. Comparison of transcripts in the parental strain and a narXL deletion mutant revealed that transcription of 51 operons is activated, directly or indirectly, by NarL, and a further 41 operons are repressed. The narP gene was also deleted from the narXL mutant to reveal the extent of regulation by phosphorylated NarP. Fourteen promoters were more active in the narP+ strain than in the mutant, and a further 37 were strongly repressed. This is the first report that NarP might function as a global repressor as well as a transcription activator. The data also revealed possible new defense mechanisms against reactive nitrogen species.

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NarZYW is constitutively expressed at low levels in the aerobic setting and only up-regulated in response to high nitrate concentrations, likely aiding in the transition from aerobic to anaerobic respiration.
“Conversely, NarZYW is constitutively expressed at low levels in the aerobic setting and only up-regulated in response to high nitrate concentrations, likely aiding in the transition from aerobic to anaerobic respiration [256,259,260].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [259]

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Authors: Constantinidou, C., Hobman, J. L., Griffiths, L., Patel, M. D., Penn, C. W., Cole, J. A., & Overton, T. W.
Affiliations: University of Birmingham (GB)
Corresponding author: Overton, Tim W.
ORCID: Constantinidou, Chrystala
Hobman, Jon L.
Cole, Jeffrey A.
Overton, Tim W.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2006-02
Volume: 281
Issue: 8
Pages: 4802-4815
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m512312200
OpenAlex: W2158718811
Cited by: 280
References: 89
Citations by year: 2026: 5 · 2025: 8 · 2024: 7 · 2023: 8 · 2022: 15 · 2021: 13 · 2020: 7 · 2019: 17 · 2018: 6 · 2017: 11 · 2016: 14 · 2015: 12 · 2014: 19 · 2013: 14 · 2012: 15
FWCI: 7.91
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 5400 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed (publishedVersion)
Repository@Nottingham (University of Nottingham) (submittedVersion, other-oa)
Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
Funders: Directorate for Biological Sciences
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Keywords: Escherichia coli K-12, nitrate regulation, NARP, NarL, fumarate reduction, operon regulation, trimethylamine N-oxide
MeSH terms: Binding Sites, DNA-Binding Proteins, Escherichia coli, Glucose, Iron-Sulfur Proteins, Membrane Proteins, Models, Biological, Mutation, Nitrates, Nitrites, Nucleic Acid Hybridization, Oxygen, Phosphoproteins, Promoter Regions, Genetic, Protein Kinases, Time Factors, Transcriptional Activation, Genome, Bacterial, Gene Deletion, DNA Primers, Oligonucleotide Array Sequence Analysis, Escherichia coli Proteins, Chromatin Immunoprecipitation

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A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth

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