The ferric enterobactin transporter Fep is required for persistent Salmonella enterica serovar Typhimurium infection

Nagy, Toni A.; Moreland, Sarah M.; Andrews-Polymenis, Helene; Detweiler, Corrella S.

doi:10.1128/iai.00412-13

Cited by 72Salmonella and Campylobacter epidemiologyBacterial Genetics and BiotechnologyEscherichia coli research studies

The ferric enterobactin transporter Fep is required for persistent Salmonella enterica serovar Typhimurium infection

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Nagy, Toni A., Moreland, Sarah M., Andrews-Polymenis, Helene, Detweiler, Corrella S.·2013·Infection and Immunity

DOI 10.1128/iai.00412-13PMC PMC3811836

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Abstract

Most bacterial pathogens require iron to grow and colonize host tissues. The Gram-negative bacterium Salmonella enterica serovar Typhimurium causes a natural systemic infection of mice that models acute and chronic human typhoid fever. S. Typhimurium resides in tissues within cells of the monocyte lineage, which limit pathogen access to iron, a mechanism of nutritional immunity. The primary ferric iron import system encoded by Salmonella is the siderophore ABC transporter FepBDGC. The Fep system has a known role in acute infection, but it is unclear whether ferric iron uptake or the ferric iron binding siderophores enterobactin and salmochelin are required for persistent infection. We defined the role of the Fep iron transporter and siderophores in the replication of Salmonella in macrophages and in mice that develop acute followed by persistent infections. Replication of wild-type and iron transporter mutant Salmonella strains was quantified in cultured macrophages, fecal pellets, and host tissues in mixed- and single-infection experiments. We show that deletion of fepB attenuated Salmonella replication and colonization within macrophages and mice. Additionally, the genes required to produce and transport enterobactin and salmochelin across the outer membrane receptors, fepA and iroN, are needed for colonization of all tissues examined. However, salmochelin appears to be more important than enterobactin in the colonization of the spleen and liver, both sites of dissemination. Thus, the FepBDGC ferric iron transporter and the siderophores enterobactin and salmochelin are required by Salmonella to evade nutritional immunity in macrophages and cause persistent infection in mice.

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NTS within phagocytic cells acquires ferrous and ferric iron by upregulating FeoB or FepB and the siderophores enterochelin and salmochelin.
“Once infected, NTS within phagocytic cells acquires ferrous and ferric iron by upregulating expression of the iron importers FeoB or FepB, respectively, (Nagy et al., 2014) and the siderophores enterochelin and salmochelin (Nagy et al., 2013).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Nagy et al., 2013

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<scp>S</scp>almonellaacquires ferrous iron from haemophagocytic macrophages
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Biosynthesis and IroC‐dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium
Crouch, M. V., Castor, M., Karlinsey, J. E., Kalhorn, T., & Fang, F. C. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06089.x · Cited by 187 · see citing works

Authors: Nagy, T. A., Moreland, S. M., Andrews-Polymenis, H., & Detweiler, C. S.
Affiliations: University of Colorado Boulder (US)
Texas A&M University System Health Science Center, College Station, Texas, USA
ORCID: Nagy, Toni A.
Detweiler, Corrella S.
Venue: Infection and Immunity
Publisher: American Society for Microbiology
Published: 2013-11
Volume: 81
Issue: 11
Pages: 4063-4070
ISSN: 0019-9567 (ISSN-L)
1098-5522
DOI: 10.1128/iai.00412-13
PMC: PMC3811836
OpenAlex: W2116924544
Cited by: 72
References: 66
Citations by year: 2026: 6 · 2025: 6 · 2024: 5 · 2023: 4 · 2022: 8 · 2021: 6 · 2020: 7 · 2019: 11 · 2018: 4 · 2017: 6 · 2016: 4 · 2015: 3 · 2014: 2
FWCI: 4.48
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Infection and Immunity (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
OakTrust (Texas A&M University Libraries) (submittedVersion)
Funders: National Institutes of Health (5f32ai094766-03)
National Institute of Allergy and Infectious Diseases (R56AI095395, 1F32AI094766, R01AI095395, F32 AI094766, AI-095395, R01AI072492, AI072492)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Keywords: Salmonella typhimurium, enterobactin, salmochelin, siderophores, persistent infection, nutritional immunity, macrophages, iron, FepA, spleen colonization, liver colonization
MeSH terms: Animals, Cell Line, Disease Models, Animal, Enterobactin, Female, Liver, Macrophages, Male, Salmonella Infections, Animal, Salmonella typhimurium, Spleen, Virulence, Gene Deletion, Membrane Transport Proteins, Virulence Factors, Mice

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The ferric enterobactin transporter Fep is required for persistent Salmonella enterica serovar Typhimurium infection

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