ArticleNature communications2021
Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut.
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Article in Nature communications, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 57 papers.
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57citing papers in PubMed
9.6field-weighted citation impact, top 1% of its field
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Who cites it
57 citing papers in PubMed, 90 citations in OpenAlex.
- The Dual Role of Zinc Homeostasis in Gram-Negative Bacterial Pathogenicity and Host Immune Defense.Microorganisms · 2026Review
- Yersiniabactin-producing adherent-invasiveScience advances · 2026Article
- SLC11A2 withholds divalent metals fromProceedings of the National Academy of Sciences of the United States of America · 2026Article
- Structure-centric searching enables global mapping of the public metabolome.Nature biotechnology · 2026Article
- Aerobactin is a key driver of hypervirulent Klebsiella pneumoniae translocation and virulence.PLoS pathogens · 2026Article
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- Cellular membrane protein MipA from E.coli Nissle 1917 protects against Salmonella infection.The ISME journal · 2026Article
- High-pathogenicity island enhances NDM-5 activity and drives global spread of Escherichia coli ST410.The ISME journal · 2026Article
- Computational mass spectrometry and genome mining guided discovery of metallophores produced by Microbulbifer.ISME communications · 2026Article
- An Inflammation-Targeting Engineered Probiotic Escherichia coli Nissle 1917 with High Anti-TNF-α Nanobody Secretion Efficacy Alleviates Ulcerative Colitis.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025Article
- Multidrug resistant hypervirulent ST307 clone from genomic surveillance of extended spectrum beta-lactamase-producing Klebsiella pneumoniae species complex in East Africa.BMC microbiology · 2025Article
- SLC11A2 affects nutritional immunity in the gut epithelium.bioRxiv : the preprint server for biology · 2025Article
- Programmable conjugative CRISPR interference targeting genotoxin in the gut.Research square · 2025Article
- Programmable conjugative CRISPR interference targeting genotoxin in the gut.bioRxiv : the preprint server for biology · 2025Article
- The exploitation of nutrient metals by bacteria for survival and infection in the gut.PLoS pathogens · 2025Review
- Cross-kingdom dialogs in the gut: Integrating bacterial pathogens, helminths, and microbiota interactions for immune homeostasis.PLoS pathogens · 2025Review
- Recent advances in metallophore research uncover functions in quorum sensing, antimicrobial activity, and lanthanide acquisition.Current opinion in chemical biology · 2025Review
- Article
- Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails.Microbiome · 2025Article
- Intestinal E. coli-produced yersiniabactin promotes profibrotic macrophages in Crohn's disease.Cell host & microbe · 2025Article
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Authors and funding
26 authors at 6 institutions in 1 country.
Judith Behnsen *Department of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.ORCID http://orcid.org/0000-0003-0109-1090
Hui Zhi *Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA, 92093, USA.
Allegra T AronSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USA.
Vivekanandan SubramanianUniversity of Kentucky PharmNMR Center, College of Pharmacy, University of Kentucky, Lexington, KY, 40536-0596, USA.
William SantusDepartment of Microbiology & Immunology, University of Illinois Chicago, Chicago, IL, USA.ORCID http://orcid.org/0000-0001-5940-3769
Michael H LeeDivision of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA, 92093, USA.
Romana R GernerDivision of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA, 92093, USA.
Daniel PetrasSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USA.ORCID http://orcid.org/0000-0002-6561-3022
Janet Z LiuDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.ORCID http://orcid.org/0000-0002-9306-127X
Keith D GreenDepartment of Pharmaceutical Sciences, College of Pharmacy, University of Kentucky, Lexington, KY, 40536-0596, USA.
Sarah L PriceDepartment of Microbiology and Immunology, University of Louisville School of Medicine, Louisville, KY, 40202, USA.
Jose CamachoDivision of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA, 92093, USA.
Hannah HillmanDivision of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA, 92093, USA.
Joshua TjokrosurjoDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.
Nicola P MontaldoDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.
Evelyn M HooverDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.
Sean Treacy-AbarcaDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.
Benjamin A GilstonDepartment of Biochemistry and Chemistry, and Center for Structural Biology, Vanderbilt University Medical Center, Nashville, TN, USA.
Eric P SkaarDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.ORCID http://orcid.org/0000-0001-5094-8105
Walter J ChazinDepartment of Biochemistry and Chemistry, and Center for Structural Biology, Vanderbilt University Medical Center, Nashville, TN, USA.ORCID http://orcid.org/0000-0002-2180-0790
Sylvie Garneau-TsodikovaDepartment of Pharmaceutical Sciences, College of Pharmacy, University of Kentucky, Lexington, KY, 40536-0596, USA.
Matthew B LawrenzCenter for Predictive Medicine for Biodefense and Emerging Infectious Diseases, Department of Microbiology and Immunology, University of Louisville School of Medicine, Louisville, KY, 40202, USA.ORCID http://orcid.org/0000-0003-1505-5429
Robert D PerryDepartment of Microbiology and Immunology, University of Kentucky, Lexington, KY, 40536, USA.
Sean-Paul NuccioDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA.
Pieter C DorresteinSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USA.ORCID http://orcid.org/0000-0002-3003-1030
Manuela RaffatelluDepartment of Microbiology & Molecular Genetics, University of California Irvine, Irvine, CA, USA. manuelar@ucsd.edu.ORCID http://orcid.org/0000-0001-6487-4215
University of California, Irvine · USUniversity of California San Diego · USUniversity of Kentucky · USVanderbilt University Medical Center · USUniversity of Louisville · USUniversity of Illinois Chicago · US
Funding
Strengthening Stakeholder Engagement in Human Research Protections.UL1TR002003 · NCATS · UNIVERSITY OF ILLINOIS AT CHICAGO · PI KARNIK, NIRANJAN SUBHASH, MERMELSTEIN, ROBIN J. · 2016 to 2024
$33.7MUnderstanding the Host-Microbiome-Therapeutic Triad: Implications for Designing Alternative IntravaginalP20GM125504 · NIGMS · UNIVERSITY OF LOUISVILLE · PI HARIBABU BODDULURI · 2018 to 2026
$24.4MSystems Biology Approach to Redefine Susceptibility Testing and Treatment of MDR Pathogens in the Context of Host ImmunityU01AI124316 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI PALSSON, BERNHARD O · 2016 to 2020
$10.2MU of Calif, San Diego Neuroscience Microscopy ImagingP30NS047101 · NINDS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI GLEESON, JOSEPH G, ZHENG, BINHAI · 2003 to 2022
$9.0MTrainingP41GM103484 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI BANDEIRA, NUNO · 2012 to 2018
$8.7MHost-mediated zinc sequestration during Acinetobacter baumannii infectionR01AI101171 · NIAID · VANDERBILT UNIVERSITY MEDICAL CENTER · PI WALTER J. CHAZIN, DAVID P. GIEDROC · 2013 to 2026
$8.2MTraining Grant in GastroenterologyT32DK007202 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI GHOSH, PRADIPTA · 1985 to 2022
$7.7MC3-Dependent Intracellular Killing in Innate Immunity and Bacterial PathogenesisR01AI145325 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI NIZET, VICTOR, RAFFATELLU, MANUELA · 2019 to 2023
$3.1MIntestinal 5-HT Transporter: A novel therapeutic target for GI disordersR01DK098170 · NIDDK · UNIVERSITY OF ILLINOIS AT CHICAGO · PI GILL, RAVINDER K · 2014 to 2022
$3.0MProbing the role of commensal intestinal fungi during Salmonella pathogenesisR01AI143641 · NIAID · UNIVERSITY OF ILLINOIS AT CHICAGO · PI BEHNSEN, JUDITH · 2019 to 2023
$2.0MNutritional immunity during Salmonella infectionR01AI126277 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI RAFFATELLU, MANUELA · 2016 to 2020
$1.9MDevelopment of siderophore-based vaccines against non-typhoidal Salmonella infectionR01AI114625 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI NOLAN, ELIZABETH M, RAFFATELLU, MANUELA · 2015 to 2019
$1.9MNCATS NIH HHS UL1 TR002003NCRR NIH HHS S10 RR029121NIAID NIH HHS F31 AI147404NIAID NIH HHS R01 AI101171NIAID NIH HHS R01 AI114625NIAID NIH HHS R01 AI126277NIAID NIH HHS R01 AI143641NIAID NIH HHS R01 AI145325NIAID NIH HHS R21 AI119557NIAID NIH HHS R21 AI135225NIAID NIH HHS R37 AI126277NIAID NIH HHS R56 AI114625NIAID NIH HHS T32 AI132146NIAID NIH HHS U01 AI124316NIDDK NIH HHS R01 DK098170NIDDK NIH HHS T32 DK007202NIGMS NIH HHS P20 GM125504NIGMS NIH HHS P41 GM103484NIH HHS S10 OD028690NINDS NIH HHS P30 NS047101
Abstract
Zinc is an essential cofactor for bacterial metabolism, and many Enterobacteriaceae express the zinc transporters ZnuABC and ZupT to acquire this metal in the host. However, the probiotic bacterium Escherichia coli Nissle 1917 (or "Nissle") exhibits appreciable growth in zinc-limited media even when these transporters are deleted. Here, we show that Nissle utilizes the siderophore yersiniabactin as a zincophore, enabling Nissle to grow in zinc-limited media, to tolerate calprotectin-mediated zinc sequestration, and to thrive in the inflamed gut. We also show that yersiniabactin's affinity for iron or zinc changes in a pH-dependent manner, with increased relative zinc binding as the pH increases. Thus, our results indicate that siderophore metal affinity can be influenced by the local environment and reveal a mechanism of zinc acquisition available to commensal and pathogenic Enterobacteriaceae.
Indexed as
AnimalsATP-Binding Cassette TransportersBacterial ProteinsCarrier ProteinsColonEnterobacteriaceaeEscherichia coliEscherichia coli ProteinsFemaleLeukocyte L1 Antigen ComplexMembrane Transport ProteinsMiceMice, Inbred C57BLPhenolsSalmonella typhiSiderophoresATP-Binding Cassette TransportersBacterial ProteinsCarrier ProteinsEscherichia coli ProteinsLeukocyte L1 Antigen ComplexMembrane Transport ProteinsPhenolsSiderophoresThiazolesyersiniabactinZinczinc-binding proteinZnuA protein, E coli
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