Cited by 536Bacterial Genetics and BiotechnologyEscherichia coli research studiesIron Metabolism and Disorders

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Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor

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de Lorenzo, V, Wee, S, Herrero, M, Neilands, J B·1987·Journal of Bacteriology

DOI 10.1128/jb.169.6.2624-2630.1987PMC PMC212138

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Abstract

The promoter region of the pColV-K30-encoded operon specifying biosynthesis and transport of the siderophore aerobactin was subjected to deletion analysis to determine the smallest DNA sequence affording iron regulation of a iucA'-'lacZ gene fusion. A 78-base-pair (bp) region containing the main (P1) promoter retained the character of inducibility under iron starvation. A 250-bp fragment carrying this sequence was examined for protection against DNase I by the Fur protein, the product of a gene (fur) required for negative control of several iron-regulated functions. The DNase I footprints, in the presence of various divalent heavy-metal ions added as corepressors, revealed two contiguous binding sites with different lengths and affinities for Fur. Increased concentrations of the protein appeared to elicit formation of repressor oligomers which bind to the upstream and downstream regions of the P1 promoter in a metal-dependent fashion, but with a presently undefined stoichiometry. The primary site for Fur binding spans 31 bp and contains two overlapping symmetry dyads which share the sequence 5'-TCATT-3'. It also contains extensive homology with a 19-bp consensus sequence for iron-regulated genes as deduced from comparison with the fhuA and fepA putative promoter sequences.

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“Fur-like proteins are ubiquitous in bacteria, and act as transcriptional repressors that exhibit an iron-dependent DNA binding activity and regulate several genes involved in iron metabolism [20,21].”
TonB is essential for virulence in avian pathogenic Escherichia coli
Holden, K. M., Browning, G. F., Noormohammadi, A. H., Markham, P. F., & Marenda, M. S. (2012) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2011.12.004 · Cited by 21
Cleavage of a putative metal permease in Chlamydia trachomatis yields an iron-dependent transcriptional repressor
Thompson, C. C., Nicod, S. S., Malcolm, D. S., Grieshaber, S. S., & Carabeo, R. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201398109 · Cited by 20
“Homodimers of the metal-activated proteins recognize specific cis-regulatory elements that are often located proximally to the promoter operating regions of the regulated gene, effectively blocking RNA polymerase initiation of transcription (3, 4).”
Background
Identification and Functional Analysis of CT069 as a Novel Transcriptional Regulator in Chlamydia
Akers, J. C., HoDac, H., Lathrop, R. H., & Tan, M. (2011) · Journal of Bacteriology · doi:10.1128/jb.05976-11 · Cited by 20
“CT069 thus appears to be similar to other prokaryotic metal-dependent repressors, such as DtxR and Fur, that utilize specific divalent metal ions as cofactors (7, 18, 49).”
Molecular characterization of a heme-binding protein of Bacteroides fragilis BE1
Otto, B. R., Kusters, J. G., Luirink, J., de Graaf, F. K., & Oudega, B. (1996) · Infection and Immunity · doi:10.1128/iai.64.10.4345-4350.1996 · Cited by 20
“Under non-iron-restricted conditions, Fur binds to a highly conserved DNA sequence called the Fur box located in the operator-promoter region of iron-regulated genes and blocks transcription, whereas under iron-deprived conditions, repression by Fur is relieved and the genes are transcribed (2, 7).”
Background
A syntactic representation of units of genetic information—A syntax of units of genetic information
Collado‐Vides, J. (1991) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80245-0 · Cited by 20
Analysis of the Erwinia chrysanthemi ferrichrysobactin receptor gene: resemblance to the Escherichia coli fepA-fes bidirectional promoter region and homology with hydroxamate receptors
Sauvage, C., Franza, T., & Expert, D. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.4.1227-1231.1996 · Cited by 20
The Ferric uptake regulator (Fur) and iron availability control the production and maturation of the antibacterial peptide microcin E492
Marcoleta, A. E., Gutiérrez-Cortez, S., Hurtado, F., Argandoña, Y., Corsini, G., Monasterio, O., & Lagos, R. (2018) · PLOS ONE · doi:10.1371/journal.pone.0200835 · Cited by 19
Structural Perspectives on Metal Dependent Roles of Ferric Uptake Regulator (Fur)
Kang, S., Kang, H.-S., Chung, W., Kang, K., & Kim, D.-H. (2024) · Biomolecules · doi:10.3390/biom14080981 · Cited by 19
Expression of the Iron-ActivatednspAandsecYGenes inNeisseria meningitidisGroup B by Fur-Dependent and -Independent Mechanisms
Shaik-Dasthagirisaheb, Y. B., Grogan, S., Davey, M., Sebastian, S., Goswami, S., Szmigielski, B., & Genco, C. A. (2006) · Journal of Bacteriology · doi:10.1128/jb.01638-06 · Cited by 19
“coli palindromic Fur binding sequence (2, 9, 10) or a 21-bp Neisseria consensus sequence that has 80% homology with the E.”
Background
Algae induce siderophore biosynthesis in the freshwater bacterium Cupriavidus necator H16
Kurth, C., Wasmuth, I., Wichard, T., Pohnert, G., & Nett, M. (2018) · BioMetals · doi:10.1007/s10534-018-0159-6 · Cited by 19
Azotobacter vinelandii strains of disparate origin produce azotobactin siderophores with identical structures
Page, W. J., Collinson, S. K., Demange, P., Dell, A., & Abdallah, M. A. (1991) · BioMetals · doi:10.1007/bf01141184 · Cited by 19
Identification, isolation, and analysis of a gene cluster involved in iron acquisition by Pseudomonas mendocina ymp
Awaya, J. D., & DuBois, J. L. (2007) · BioMetals · doi:10.1007/s10534-007-9124-5 · Cited by 18
Isolation and analysis of a linear plasmid‐located gene of Borrelia burgdorferi B29 encoding a 27 kDa surface lipoprotein (P27) and its overexpression in Escherichia coli
Reindl, M., Redl, B., & Stöffler, G. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01656.x · Cited by 19
The FUR-like regulators PerRA and PerRB integrate a complex regulatory network that promotes mammalian host-adaptation and virulence of Leptospira interrogans
Grassmann, A. A., Zavala-Alvarado, C., Bettin, E. B., Picardeau, M., Benaroudj, N., & Caimano, M. J. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009078 · Cited by 16
Molecular Analysis of Iron-Deficient Graminaceous Plants
Kobayashi, T., Nishizawa, N. K., & Mori, S. (2006) · Springer eBooks · doi:10.1007/1-4020-4743-6_20 · Cited by 18
Iron control of the Vibrio fischeri luminescence system in Escherichia coli
Dunlap, P. V. (1992) · Archives of Microbiology · doi:10.1007/bf00245156 · Cited by 18
The transcriptional regulation of the horizontally acquired iron uptake system, yersiniabactin and its contribution to oxidative stress tolerance and pathogenicity of globally emerging salmonella strains
Diamant, I., Adani, B., Sylman, M., Rahav, G., & Gal‐Mor, O. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2369339 · Cited by 17
“45 Promoter architecture analysis of the ybtA-ybtP intergenic region in pESI using the VirtualFootprint tool 46 identified a similar 19 bp sequence (5’-”
Method
Divergence of the aerobactin iron uptake systems encoded by plasmids pColV-K30 in Escherichia coli K-12 and pSMN1 in Aerobacter aerogenes 62-1
Waters, V. L., & Crosa, J. H. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.11.5153-5160.1988 · Cited by 17
An electron spin resonance study of the Mn(II) and Cu(II) complexes of the Fur repressor protein
Hamed, M. Y., & Neilands, J. B. (1994) · Journal of Inorganic Biochemistry · doi:10.1016/0162-0134(94)85111-5 · Cited by 17
Self-citation
Transcriptional regulation of a second flavodoxin gene from Klebsiella pneumoniae
Achenbach, L. A., & Genova, E. G. (1997) · Gene · doi:10.1016/s0378-1119(97)00168-6 · Cited by 17
Cloning, nucleotide sequencing, and expression of the Azospirillum brasilense lon gene: involvement in iron uptake
Mori, E., Fulchieri, M., Indorato, C., Fani, R., & Bazzicalupo, M. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.12.3440-3446.1996 · Cited by 17
“coli s(70) promoter and to the iron box (7) or to the heat shock consensus promoter (20, 35) did not give any significant result.”
Background
Characterization of in-frame proteins encoded by cvaA, an essential gene in the colicin V secretion system: CvaA* stabilizes CvaA to enhance secretion
Hwang, J., Manuvakhova, M., & Tai, P. C. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.3.689-696.1997 · Cited by 16
Molecular cloning, expression, and regulation in Escherichia coli K-12 of a chromosome-mediated aerobactin iron transport system from a human invasive isolate of E. coli K1
Valvano, M. A., & Crosa, J. H. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.12.5529-5538.1988 · Cited by 16
“In the P1 promoter of pColV-K30, there is a region spanning from 7 base pairs (bp) upstream of the -35 region to the first base pair of its -10 sequence which was defined as the primary binding site for the Fur repressor protein (13).”
BackgroundInfluential
Effect of iron availability on expression of the Bradyrhizobium japonicum hemA gene
Page, K. M., Connolly, E. L., & Guerinot, M. L. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.5.1535-1538.1994 · Cited by 16
“coli which is the binding site for Fur (12).”
Background
A linguistic representation of the regulation of transcription initiation. I. An ordered array of complex symbols with distinctive features
Collado‐Vides, J. (1993) · Biosystems · doi:10.1016/0303-2647(93)90086-r · Cited by 16
Control of Bacterial Iron Transport by Regulatory Proteins
Hantke, K., & Braun, V. (1998) · Springer eBooks · doi:10.1007/978-1-4615-5993-1_2 · Cited by 16
Stimulation, purification, and chemical characterization of siderophores produced by the rhizospheric bacterial strain Pseudomonas putida
Hussein, K. A., & Joo, J. H. (2017) · Rhizosphere · doi:10.1016/j.rhisph.2017.05.006 · Cited by 15
FurC ( PerR ) from Anabaena sp. PCC7120 : a versatile transcriptional regulator engaged in the regulatory network of heterocyst development and nitrogen fixation
Sarasa‐Buisan, C., Guío, J., Broset, E., Peleato, M. L., Fillat, M. F., & Sevilla, E. (2021) · Environmental Microbiology · doi:10.1111/1462-2920.15552 · Cited by 15
“The predicted consensus suggests that FurC from Anabaena sp. PCC 7120 presumably associates with DNA at an imperfect 9-1-9 inverted motif which shares 58% homology to the classical 9-1-9 inverted consensus sequence from E. coli Fur: 50- GATAATGATAATCATTATC-30 (de Lorenzo et al., 1987).”
Background
Gene cluster for ferric iron uptake in Agrobacterium tumefaciens MAFF301001.
Sonoda, H., Suzuki, K., & Yoshida, K. (2002) · Genes & Genetic Systems · doi:10.1266/ggs.77.137 · Cited by 15
“The iron box is Fur (ferric uptake regulator) protein binding site and an upstream regulatory sequence, which is a 19- bp palindromic sequence in E. coli (De Lorenzo et al., 1987).”
Background
Microarray Analysis of Mycobacterium bovis BCG Revealed Induction of Iron Acquisition Related Genes in Response to Hydrogen Peroxide.
Jang, H.-J., Nde, C. W., Toghrol, F., & Bentley, W. E. (2009) · Environmental Science & Technology · doi:10.1021/es902255q · Cited by 15
Identification of Btr-regulated genes using a titration assay. Search for a role for this transcriptional regulator in the growth and virulence of Bordetella pertussis
Wood, G. E., Khelef, N., Guiso, N., & Friedman, R. L. (1998) · Gene · doi:10.1016/s0378-1119(98)00031-6 · Cited by 15
Transcriptional Control of the rhuIR-bhuRSTUV Heme Acquisition Locus in Bordetella avium
King, N. D., Kirby, A. E., & Connell, J. W. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1613-1624.2005 · Cited by 15
“In its repressor mode, Fe-bound Fur has affinity for the Fur box, a consensus motif that is located within or near Fur-regulated promoters (7).”
Background

Authors: de Lorenzo, V, Wee, S., Herrero, M., & Neilands, J. B.
Affiliations: University of California, Berkeley (US)
Venue: Journal of Bacteriology
Publisher: American Society for Microbiology
Published: 1987-06
Volume: 169
Issue: 6
Pages: 2624-2630
ISSN: 0021-9193 (ISSN-L)
1098-5530
DOI: 10.1128/jb.169.6.2624-2630.1987
PMC: PMC212138
OpenAlex: W2131282911
Cited by: 536
References: 22
Citations by year: 2026: 2 · 2025: 3 · 2024: 7 · 2023: 5 · 2022: 6 · 2021: 8 · 2020: 9 · 2019: 4 · 2018: 8 · 2017: 6 · 2016: 13 · 2015: 12 · 2014: 11 · 2013: 9 · 2012: 21
FWCI: 14.06
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Bacteriology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Ministerio de Economía y Competitividad
National Institutes of Health (1f05tw003577-01)
U.S. Public Health Service (A104156)
Fogarty International Center (1F05TWO3577-01-BI-5)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Keywords: Fur repressor, iron regulation, promoter, DNase I footprinting, repressor binding sites, consensus sequence, siderophore biosynthesis, Escherichia coli
MeSH terms: Bacterial Proteins, Chromosome Deletion, Cloning, Molecular, Bacteriocin Plasmids, Escherichia coli, Gene Expression Regulation, Hydroxamic Acids, Iron, Operator Regions, Genetic, Operon, Promoter Regions, Genetic, Recombinant Fusion Proteins, Repressor Proteins, Transcription Factors

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Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor

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