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Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron
Open accessAbstract
Host inflammation alters the availability of nutrients such as iron to limit microbial growth. However, Salmonella enterica serovar Typhimurium thrives in the inflamed gut by scavenging for iron with siderophores. By administering Escherichia coli strain Nissle 1917, which assimilates iron by similar mechanisms, we show that this nonpathogenic bacterium can outcompete and reduce S. Typhimurium colonization in mouse models of acute colitis and chronic persistent infection. This probiotic activity depends on E. coli Nissle iron acquisition, given that mutants deficient in iron uptake colonize the intestine but do not reduce S. Typhimurium colonization. Additionally, the ability of E. coli Nissle to overcome iron restriction by the host protein lipocalin 2, which counteracts some siderophores, is essential, given that S. Typhimurium is unaffected by E. coli Nissle in lipocalin 2-deficient mice. Thus, iron availability impacts S. Typhimurium growth, and E. coli Nissle reduces S. Typhimurium intestinal colonization by competing for this limiting nutrient.
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In the citing paper
“In doing so, NGAL maintains the balance between commensal bacteria and immune cells in the gut where colitogenic bacteria can reside and secrete high amounts of enterobactin into the intestinal lumen (Deriu et al., 2013;Moschen et al., 2016;Toyonaga et al., 2016).”
From Iron in infection and immunity (2020) · cites this paper as Deriu et al., 2013
Experimental — accuracy not yet measuredIn the citing paper
“The probiotic bacterium E. coli Nissle 1917 (EcN) encodes mechanisms to uptake exogenous iron and heme as well as the siderophores yersiniabactin, aerobactin, and salmochelin (Deriu et al., 2013).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Deriu et al., 2013
In the citing paper
“EcN is able to outcompete and suppress S. Typhimurium colonization in an iron-dependent manner and only in the presence of lipocalin-2 (Deriu et al., 2013)”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Deriu et al., 2013
In the citing paper
“Lipocalin 2 (LCN2) is a host antimicrobial factor induced upon infection that inhibits bacterial uptake of iron-laden siderophores (Flo et al., 2004, Raffatellu et al., 2009, Deriu et al., 2013).”
From Iron Regulatory Proteins Mediate Host Resistance to Salmonella Infection (2015) · cites this paper as Deriu et al., 2013
In the citing paper
“Delivery of Lcn2 by probiotic bacteria has also been shown to control Salmonella infection [235].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [235]
In the citing paper
“EcN is believed to impede the growth of opportunistic pathogens, including Salmonella spp. and other coliform enteropathogens, through the production of microcin proteins or production of iron-scavenging siderophores18,22,23.”
From Developing a new class of engineered live bacterial therapeutics to treat human diseases (2020) · cites this paper as [23]
In the citing paper
“The authors demonstrated that Nissle is able to suppress gastroenteritis induced by Salmonella enterica serovar Typhimurium through competition for iron [82].”
From Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy (2015) · cites this paper as [82]
In the citing paper
“The ability of Nissle to outcompete S. enterica was also dependent on the presence of the host siderophore-binding protein lipocalin 2, illustrating a complex interplay among host, pathogen, and commensal species.”
From Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy (2015) · cites this paper as [82]
In the citing paper
“Specific strains of commensal bacteria are particularly adept at competing with pathogens for iron, even under inflammatory conditions when host‐imposed iron limitation ‐ through increased production of LCN2 and Lf – can disadvantage the microbiota as a whole.”
From The battle for iron in enteric infections (2020) · cites this paper as [169]
In the citing paper
“The non‐pathogenic E. coli strain Nissle has complex iron acquisition pathways and can secrete and utilize not only enterobactin, but also LCN2‐resistant salmochelin, yersiniabactin and aerobactin to effectively acquire iron at the expense of Salmonella. 17 , 168 , 169”
From The battle for iron in enteric infections (2020) · cites this paper as [169]
In the citing paper
“During S. enterica gastrointestinal infection, S. enterica uses salmochelin to gain a competitive advantage over commensals but is outcompeted for siderophores by the probiotic E. coli strain Nissle, which reduces S. enterica colonization (33, 113).”
From Transition Metals and Virulence in Bacteria (2016) · cites this paper as [33]
In the citing paper
“However, bacteria can also compete for other compounds that support their growth, such as iron and zinc reservoirs [69, 70].”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [69]
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Metadata
- Authors
- Deriu, E., Liu, J. Z., Pezeshki, M., Edwards, R. A., Ochoa, R. J., Contreras, H., Libby, S. J., Fang, F. C., & Raffatellu, M.
- Affiliations
- University of California, Irvine (US)
- University of Washington (US)
- Corresponding author
- Raffatellu, Manuela
- ORCID
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 14
- Issue
- 1
- Pages
- 26-37
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3752295
- OpenAlex
- W1966223820
- Cited by
- 550
- References
- 64
- Citations by year
- 2026: 44 · 2025: 57 · 2024: 46 · 2023: 51 · 2022: 60 · 2021: 49 · 2020: 51 · 2019: 45 · 2018: 33 · 2017: 29 · 2016: 28 · 2015: 25 · 2014: 26 · 2013: 5
- FWCI
- 41.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (AI77629, AI083663, T32 AI60573, R01AI077629, R01AI083663, T32AI060573, U54AI065359)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- probiotics, Salmonella typhimurium, Escherichia coli Nissle 1917, iron acquisition, siderophores, neutrophil gelatinase-associated lipocalin, intestinal colonization, acute colitis, persistent infection, host inflammatory response, nutrient competition, host-pathogen interaction
- MeSH terms
- Animals, Colitis, Escherichia coli, Female, Humans, Intestinal Mucosa, Intestines, Iron, Mice, Inbred C57BL, Salmonella Infections, Salmonella typhimurium, Probiotics, Mice
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