Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron

Deriu, Elisa; Liu, Janet Z.; Pezeshki, Milad; Edwards, Robert A.; Ochoa, Roxanna J.; Contreras, Heidi; Libby, Stephen J.; Fang, Ferric C.; Raffatellu, Manuela

doi:10.1016/j.chom.2013.06.007

Cited by 555Probiotics and Fermented FoodsSalmonella and Campylobacter epidemiologyBacterial Genetics and Biotechnology

Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron

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Deriu, Elisa, Liu, Janet Z., Pezeshki, Milad, Edwards, Robert A., Ochoa, Roxanna J., Contreras, Heidi, Libby, Stephen J., Fang, Ferric C. +1 more·2013·Cell Host & Microbe

DOI 10.1016/j.chom.2013.06.007PMC PMC3752295

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Abstract

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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By binding enterobactin, 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.
“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
The Introduction (page unavailable) says lipocalin-2 sequesters iron-bound enterochelin (enterobactin), and the Results describe how this affects commensal E. coli and Salmonella in the inflamed gut. The paper does not establish that NGAL thereby maintains a balance between commensal bacteria and immune cells, or that colitogenic bacteria secrete high amounts of enterobactin into the intestinal lumen. (LLM, conf=0.86)
Experimental — accuracy not yet measured
E. coli Nissle 1917 encodes mechanisms to take up exogenous iron and heme and to use the siderophores yersiniabactin, aerobactin, and salmochelin.
“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
EcN outcompetes and suppresses S. Typhimurium colonization in an iron-dependent manner and only when lipocalin-2 is present.
“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
LCN2 is an infection-induced host antimicrobial that blocks bacterial uptake of iron-loaded siderophores.
“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
Delivery of Lcn2 by probiotic bacteria controls Salmonella infection.
“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]

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 siderophores.
“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]
Nissle suppresses Salmonella Typhimurium gastroenteritis by competing for iron.
“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]
Nissle's ability to outcompete S. enterica requires the host siderophore-binding protein lipocalin 2.
“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]
Specific strains of commensal bacteria are particularly adept at competing with pathogens for iron, even under inflammatory conditions when host-imposed iron limitation can disadvantage the microbiota as a whole.
“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]
The non-pathogenic E. coli strain Nissle has complex iron acquisition pathways and can secrete and utilize enterobactin, LCN2-resistant salmochelin, yersiniabactin and aerobactin to effectively acquire iron at the expense of Salmonella.
“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]
During Salmonella enterica gastrointestinal infection, salmochelin provides a competitive advantage over commensals, but the probiotic E. coli strain Nissle outcompetes S. enterica for siderophores and reduces its colonization.
“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]
Bacteria can also compete for other compounds that support their growth, such as iron and zinc reservoirs.
“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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Dysbiosis and the immune system
Levy, M., Kolodziejczyk, A. A., Thaiss, C. A., & Elinav, E. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.7 · Cited by 1,769 · see citing works
Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease
Pickard, J. M., Zeng, M. Y., Caruso, R., & Núñez, G. (2017) · Immunological Reviews · doi:10.1111/imr.12567 · Cited by 1,699 · see citing works
Interactions between the microbiota and pathogenic bacteria in the gut
Bäumler, A. J., & Sperandio, V. (2016) · Nature · doi:10.1038/nature18849 · Cited by 1,420 · see citing works
Bacterial siderophores in community and host interactions
Kramer, J., Özkaya, Ö., & Kümmerli, R. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0284-4 · Cited by 998 · see citing works
Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature
Fijan, S. (2014) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph110504745 · Cited by 1,059 · see citing works
Mechanisms of inflammation-driven bacterial dysbiosis in the gut
Zeng, M. Y., Inohara, N., & Núñez, G. (2016) · Mucosal Immunology · doi:10.1038/mi.2016.75 · Cited by 872 · see citing works
Microcins mediate competition among Enterobacteriaceae in the inflamed gut
Sassone-Corsi, M., Nuccio, S.-P., Liu, H., Hernandez, D., Vu, C. T., Takahashi, A. A., Edwards, R. A., & Raffatellu, M. (2016) · Nature · doi:10.1038/nature20557 · Cited by 549 · see citing works
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Gut Microbiota and Colonization Resistance against Bacterial Enteric Infection
Ducarmon, Q. R., Zwittink, R. D., Hornung, B. V. H., van Schaik, W., Young, V. B., & Kuijper, E. J. (2019) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00007-19 · Cited by 566 · see citing works
Developing a new class of engineered live bacterial therapeutics to treat human diseases
Charbonneau, M. R., Isabella, V. M., Li, N., & Kurtz, C. B. (2020) · Nature Communications · doi:10.1038/s41467-020-15508-1 · Cited by 523 · see citing works
A Gut Commensal-Produced Metabolite Mediates Colonization Resistance to Salmonella Infection
Jacobson, A., Lam, L., Rajendram, M., Tamburini, F., Honeycutt, J., Pham, T., Van Treuren, W., Pruss, K., Stabler, S. R., Lugo, K., et al. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.07.002 · Cited by 507 · see citing works
Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium
Brugiroux, S., Beutler, M., Pfann, C., Garzetti, D., Ruscheweyh, H., Ring, D., Diehl, M., Herp, S., Loetscher, Y., Hussain, S., et al. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.215 · Cited by 463 · see citing works
Transition Metals and Virulence in Bacteria
Palmer, L. D., & Skaar, E. P. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-120215-035146 · Cited by 449 · see citing works
Microbiota-mediated colonization resistance: mechanisms and regulation
Caballero-Flores, G., Pickard, J. M., & Núñez, G. (2023) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00833-7 · Cited by 474 · see citing works
Immunological mechanisms of inflammatory diseases caused by gut microbiota dysbiosis: A review
Zhao, M., Chu, J., Feng, S., Guo, C., Xue, B., He, K., & Li, L. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114985 · Cited by 466 · see citing works
Lipocalin 2: an emerging player in iron homeostasis and inflammation
Xiao, X., Yeoh, B. S., & Vijay-Kumar, M. (2017) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071816-064559 · Cited by 426 · see citing works
Lipocalin 2 protects from inflammation and Tumorigenesis associated with gut microbiota alterations
Moschen, A. R., Gerner, R. R., Wang, J., Klepsch, V., Adolph, T. E., Reider, S. J., Hackl, H., Pfister, A., Schilling, J., Moser, P. L., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.03.007 · Cited by 375 · see citing works
Microbial nutrient niches in the gut
Pereira, F. C., & Berry, D. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13659 · Cited by 365 · see citing works
Iron in infection and immunity
Nairz, M., & Weiss, G. (2020) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2020.100864 · Cited by 359 · see citing works
Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence
Porcheron, G., Garénaux, A., Proulx, J., Sabri, M., & Dozois, C. M. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00090 · Cited by 367 · see citing works
Engineering living therapeutics with synthetic biology
Cubillos-Ruiz, A., Guo, T., Sokolovska, A., Miller, P., Collins, J. J., Lu, T. K., & Lora, J. M. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00285-3 · Cited by 371 · see citing works
Anti-Infective Activities of Lactobacillus Strains in the Human Intestinal Microbiota: from Probiotics to Gastrointestinal Anti-Infectious Biotherapeutic Agents
Moal, V. L.-L., & Servin, A. L. (2014) · Clinical Microbiology Reviews · doi:10.1128/cmr.00080-13 · Cited by 355 · see citing works
Iron at the interface of immunity and infection
Nairz, M., Haschka, D., Demetz, E., & Weiss, G. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00152 · Cited by 325 · see citing works
“IFN-γ induces the expression of Nramp1, Lcn2, and NO thereby reducing intracellular iron content in macrophages and limiting the growth of bacteria such as Salmonella (Gruenheid et al., 1997; Fritsche et al., 2008; Nairz et al., 2008, 2009a; Andrews-Polymenis et al., 2010; Nairz et al., 2013).”
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No Vacancy: How Beneficial Microbes Cooperate with Immunity To Provide Colonization Resistance to Pathogens
Sassone‐Corsi, M., & Raffatellu, M. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1403169 · Cited by 330 · see citing works
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Escherichia coli strain Nissle 1917—from bench to bedside and back: history of a special Escherichia coli strain with probiotic properties
Sonnenborn, U. (2016) · FEMS Microbiology Letters · doi:10.1093/femsle/fnw212 · Cited by 315 · see citing works
Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them
Sorbara, M. T., & Pamer, E. G. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0053-0 · Cited by 325 · see citing works
Immune homeostasis, dysbiosis and therapeutic modulation of the gut microbiota
Peterson, C. T., Sharma, V., Elmén, L., & Peterson, S. N. (2014) · Clinical & Experimental Immunology · doi:10.1111/cei.12474 · Cited by 318 · see citing works
Mucispirillum schaedleri Antagonizes Salmonella Virulence to Protect Mice against Colitis
Herp, S., Brugiroux, S., Garzetti, D., Ring, D., Jochum, L. M., Beutler, M., Eberl, C., Hussain, S., Walter, S., Gerlach, R. G., et al. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.03.004 · Cited by 312 · see citing works
Microbiome therapeutics — Advances and challenges
Mimee, M., Citorik, R. J., & Lu, T. K. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2016.04.032 · Cited by 317 · see citing works
Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans
Caza, M., & Kronstad, J. W. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00080 · Cited by 306 · see citing works
Beyond pathogens: microbiota interactions with the plant immune system
Teixeira, P. J. P. L., Colaianni, N. R., Fitzpatrick, C. R., & Dangl, J. L. (2019) · Current Opinion in Microbiology · doi:10.1016/j.mib.2019.08.003 · Cited by 314 · see citing works
Diverging roles of bacterial siderophores during infection
Holden, V. I., & Bachman, M. A. (2015) · Metallomics · doi:10.1039/c4mt00333k · Cited by 274 · see citing works
Identification of probiotic effector molecules: present state and future perspectives
Lebeer, S., Bron, P. A., Marco, M. L., van Pijkeren, J., Motherway, M. O., Hill, C., Pot, B., Roos, S., & Klaenhammer, T. R. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.10.007 · Cited by 295 · see citing works
Influenza Virus Affects Intestinal Microbiota and Secondary Salmonella Infection in the Gut through Type I Interferons
Deriu, E., Boxx, G. M., He, X., Pan, C., Benavidez, S. D., Cen, L., Rozengurt, N., Shi, W., & Cheng, G. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005572 · Cited by 280 · see citing works
Self-citation
Pollution by Antibiotics and Antimicrobial Resistance in LiveStock and Poultry Manure in China, and Countermeasures
Tian, M., He, X., Feng, Y., Wang, W., Chen, H., Gong, M., Liu, D., Clarke, J. L., & van Eerde, A. (2021) · Antibiotics · doi:10.3390/antibiotics10050539 · Cited by 277 · see citing works
Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes
Zhang, C., Derrien, M., Levenez, F., Brazeilles, R., Ballal, S. A., Kim, J., Degivry, M.-C., Quéré, G., Garault, P., van Hylckama Vlieg, J. E. T., et al. (2016) · The ISME Journal · doi:10.1038/ismej.2016.13 · Cited by 264 · see citing works
Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition
Litvak, Y., Mon, K. K. Z., Nguyen, H., Chanthavixay, G., Liou, M. J., Velazquez, E. M., Kutter, L., Alcantara, M. A., Byndloss, M. X., Tiffany, C. R., et al. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2018.12.003 · Cited by 270 · see citing works
Clostridium difficile and the microbiota
Seekatz, A. M., & Young, V. B. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72336 · Cited by 255 · see citing works
Microbiota Metabolites in Health and Disease
McCarville, J. L., Chen, G. Y., Cuevas, V. D., Troha, K., & Ayres, J. S. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-071219-125715 · Cited by 251 · see citing works
The Evolving Erythrocyte: Red Blood Cells as Modulators of Innate Immunity
Anderson, H. L., Brodsky, I. E., & Mangalmurti, N. S. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1800565 · Cited by 236 · see citing works
The Roles of Inflammation, Nutrient Availability and the Commensal Microbiota in Enteric Pathogen Infection
Stecher, B. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mbp-0008-2014 · Cited by 235 · see citing works
The Iron age of host–microbe interactions
Soares, M. P., & Weiss, G. (2015) · The EMBO Reports · doi:10.15252/embr.201540558 · Cited by 227 · see citing works
Neutrophils: from IBD to the gut microbiota
Danne, C., Skerniškytė, J., Marteyn, B. S., & Sokol, H. (2023) · Nature reviews: Gastroenterology & hepatology · doi:10.1038/s41575-023-00871-3 · Cited by 227 · see citing works
Metal limitation and toxicity at the interface between host and pathogen
Becker, K. W., & Skaar, E. P. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12087 · Cited by 223 · see citing works
Endogenous Enterobacteriaceae underlie variation in susceptibility to Salmonella infection
Velazquez, E. M., Nguyen, H., Heasley, K. T., Saechao, C. H., Gil, L. M., Rogers, A. W. L., Miller, B. M., Rolston, M. R., Lopez, C. A., Litvak, Y., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0407-8 · Cited by 201 · see citing works
Siderophore-mediated iron acquisition and modulation of host-bacterial interactions
Ellermann, M., & Arthur, J. C. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.10.489 · Cited by 186 · see citing works
The Impact of Dietary Transition Metals on Host-Bacterial Interactions
Lopez, C. A., & Skaar, E. P. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.05.008 · Cited by 190 · see citing works
Physiologically Inspired Mucin Coated Escherichia coli Nissle 1917 Enhances Biotherapy by Regulating the Pathological Microenvironment to Improve Intestinal Colonization
Yang, X., Yang, J., Ye, Z., Zhang, G., Nie, W., Cheng, H., Peng, M., Zhang, K., Liu, J., Zhang, Z., et al. (2022) · ACS Nano · doi:10.1021/acsnano.1c09681 · Cited by 197 · see citing works
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Escherichia coli Residency in the Gut of Healthy Human Adults
Martinson, J. N. V., & Walk, S. T. (2020) · EcoSal Plus · doi:10.1128/ecosalplus.esp-0003-2020 · Cited by 197 · see citing works
The cross talk between microbiota and the immune system: metabolites take center stage
Shapiro, H., Thaiss, C. A., Levy, M., & Elinav, E. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.07.003 · Cited by 189 · see citing works
Salmonellae PhoPQ regulation of the outer membrane to resist innate immunity
Dalebroux, Z. D., & Miller, S. I. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.12.005 · Cited by 186 · see citing works
Protective Microbiota: From Localized to Long-Reaching Co-Immunity
Chiu, L., Bazin, T., Truchetet, M., Schaeverbeke, T., Delhaès, L., & Pradeu, T. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01678 · Cited by 192 · see citing works
Iron Supplementation Influence on the Gut Microbiota and Probiotic Intake Effect in Iron Deficiency—A Literature-Based Review
Rusu, I. G., Suharoschi, R., Vodnar, D. C., Pop, C. R., Socaci, S. A., Vulturar, R., Istrati, M., Moroșan, I., Fărcaș, A. C., Kerezsi, A. D., et al. (2020) · Nutrients · doi:10.3390/nu12071993 · Cited by 185 · see citing works
Roles of the intestinal microbiota in pathogen protection
Úbeda, C., Djuković, A., & Isaac, S. (2017) · Clinical & Translational Immunology · doi:10.1038/cti.2017.2 · Cited by 180 · see citing works
Salmonella Mitigates Oxidative Stress and Thrives in the Inflamed Gut by Evading Calprotectin-Mediated Manganese Sequestration
Diaz-Ochoa, V. E., Lam, D., Lee, C. S., Klaus, S., Behnsen, J., Liu, J. Z., Chim, N., Nuccio, S.-P., Rathi, S. G., Mastroianni, J. R., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.05.005 · Cited by 164 · see citing works
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E. coli enhance colonization resistance against Salmonella Typhimurium by competing for galactitol, a context-dependent limiting carbon source
Eberl, C., Weiß, A. S., Jochum, L. M., Raj, A. C. D., Ring, D., Hussain, S., Herp, S., Meng, C., Kleigrewe, K., Gigl, M., et al. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.09.004 · Cited by 162 · see citing works
Microbial Activities and Intestinal Homeostasis: A Delicate Balance Between Health and Disease
Ohland, C., & Jobin, C. (2014) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2014.11.004 · Cited by 172 · see citing works
Microbiota responses to different prebiotics are conserved within individuals and associated with habitual fiber intake
Holmes, Z. C., Villa, M. M., Durand, H. K., Jiang, S., Dallow, E. P., Petrone, B. L., Silverman, J. D., Lin, P., & David, L. A. (2022) · Microbiome · doi:10.1186/s40168-022-01307-x · Cited by 177 · see citing works
Pathogens, microbiome and the host: emergence of the ecological Koch's postulates
Vonaesch, P., Anderson, M. C., & Sansonetti, P. J. (2018) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy003 · Cited by 170 · see citing works
Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome
Borton, M. A., Sabag-Daigle, A., Wu, J., Solden, L. M., O’Banion, B. S., Daly, R. A., Wolfe, R. A., Gonzalez, J. F., Wysocki, V. H., Ahmer, B. M. M., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0264-8 · Cited by 149 · see citing works
Cross-Domain and Viral Interactions in the Microbiome
Rowan-Nash, A. D., Korry, B. J., Mylonakis, E. E., & Belenky, P. A. (2019) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00044-18 · Cited by 164 · see citing works
Bacterial Quorum-Sensing Systems and Their Role in Intestinal Bacteria-Host Crosstalk
Wu, L., & Luo, Y. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.611413 · Cited by 163 · see citing works
Iron Acquisition Systems of Gram-negative Bacterial Pathogens Define TonB-Dependent Pathways to Novel Antibiotics
Klebba, P. E., Newton, S. M. C., Six, D. A., Kumar, A., Yang, T., Nairn, B. L., Munger, C., & Chakravorty, S. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c01005 · Cited by 150 · see citing works
Recipient factors in faecal microbiota transplantation: one stool does not fit all
Danne, C., Rolhion, N., & Sokol, H. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00441-5 · Cited by 154 · see citing works
Antivirulence Properties of Probiotics in Combating Microbial Pathogenesis
Nair, M. S., Amalaradjou, M. A. R., & Venkitanarayanan, K. (2017) · Advances in applied microbiology · doi:10.1016/bs.aambs.2016.12.001 · Cited by 154 · see citing works
Dietary Lactobacillus -Derived Exopolysaccharide Enhances Immune-Checkpoint Blockade Therapy
Kawanabe-Matsuda, H., Takeda, K., Nakamura, M., Makino, S., Karasaki, T., Kakimi, K., Nishimukai, M., Ohno, T., Omi, J., Kano, K., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0929 · Cited by 157 · see citing works
Iron in the Tumor Microenvironment-Connecting the Dots
Pfeifhofer-Obermair, C., Tymoszuk, P., Petzer, V., Weiss, G., & Nairz, M. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00549 · Cited by 151 · see citing works
The Pyromaniac Inside You: Salmonella Metabolism in the Host Gut
Rivera-Chávez, F., & Bäumler, A. J. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104108 · Cited by 143 · see citing works
Escherichia coli limits Salmonella Typhimurium infections after diet shifts and fat-mediated microbiota perturbation in mice
Wotzka, S. Y., Kreuzer, M., Maier, L., Arnoldini, M., Nguyen, B. D., Brachmann, A. O., Berthold, D. L., Zünd, M., Hausmann, A., Bakkeren, E., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0568-5 · Cited by 139 · see citing works
Insights from 100 years of research with probiotic E. coli
Wassenaar, T. M. (2016) · European Journal of Microbiology and Immunology · doi:10.1556/1886.2016.00029 · Cited by 147 · see citing works
Crossing the Intestinal Barrier via Listeria Adhesion Protein and Internalin A
Drolia, R., & Bhunia, A. K. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2018.12.007 · Cited by 144 · see citing works
Exploiting host immunity: the Salmonella paradigm
Behnsen, J., Pérez-López, A., Nuccio, S., & Raffatellu, M. (2015) · Trends in Immunology · doi:10.1016/j.it.2014.12.003 · Cited by 137 · see citing works
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The Quest for Novel Antimicrobial Compounds: Emerging Trends in Research, Development, and Technologies
Mantravadi, P. K., Kalesh, K., Dobson, R. C. J., Hudson, A. O., & Parthasarathy, A. (2019) · Antibiotics · doi:10.3390/antibiotics8010008 · Cited by 141 · see citing works
The microbial ecology of Escherichia coli in the vertebrate gut
Foster-Nyarko, E., & Pallen, M. J. (2022) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuac008 · Cited by 146 · see citing works
Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis
Diaz-Ochoa, V. E., Jellbauer, S., Klaus, S., & Raffatellu, M. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00002 · Cited by 129 · see citing works
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Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy
Barber, M. F., & Elde, N. C. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.09.001 · Cited by 118 · see citing works
Role of divalent metals in infectious disease susceptibility and outcome
Weiss, G., & Carver, P. L. (2018) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2017.01.018 · Cited by 123 · see citing works
Nutritional Immunity
Hennigar, S. R., & McClung, J. P. (2016) · American Journal of Lifestyle Medicine · doi:10.1177/1559827616629117 · Cited by 128 · see citing works
Klebsiella michiganensis transmission enhances resistance to Enterobacteriaceae gut invasion by nutrition competition
Oliveira, R. A., Ng, K. M., Correia, M. B., Cabral, V., Shi, H., Sonnenburg, J. L., Huang, K. C., & Xavier, K. B. (2020) · Nature Microbiology · doi:10.1038/s41564-019-0658-4 · Cited by 124 · see citing works
The Chelating Ability of Plant Polyphenols Can Affect Iron Homeostasis and Gut Microbiota
Scarano, A., Laddomada, B., Blando, F., Santis, S. D., Verna, G., Chieppa, M., & Santino, A. (2023) · Antioxidants · doi:10.3390/antiox12030630 · Cited by 130 · see citing works
Editing of the gut microbiota reduces carcinogenesis in mouse models of colitis-associated colorectal cancer
Zhu, W., Miyata, N., Winter, M. G., Arenales, A., Hughes, E. R., Spiga, L., Kim, J., Sifuentes-Dominguez, L., Starokadomskyy, P., Gopal, P., et al. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20181939 · Cited by 124 · see citing works
Iron and innate antimicrobial immunity-depriving the pathogen, defending the host
Nairz, M., Dichtl, S., Schroll, A., Haschka, D., Tymoszuk, P., Theurl, I., & Weiss, G. (2018) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2018.03.007 · Cited by 123 · see citing works
Deciphering interactions between the gut microbiota and the immune system via microbial cultivation and minimal microbiomes
Clavel, T., Neto, J. C. G., Lagkouvardos, I., & Ramer‐Tait, A. E. (2017) · Immunological Reviews · doi:10.1111/imr.12578 · Cited by 125 · see citing works
Probiotic Escherichia coli NISSLE 1917 for inflammatory bowel disease applications
Zhao, Z., Xu, S., Zhang, W., Wu, D., & Yang, G. (2022) · Food & Function · doi:10.1039/d2fo00226d · Cited by 113 · see citing works
Rethinking Diet to Aid Human–Microbe Symbiosis
Derrien, M., & Veiga, P. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.09.011 · Cited by 112 · see citing works
Immune-Microbiota Interplay and Colonization Resistance in Infection
Leshem, A., Liwinski, T., & Elinav, E. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.03.001 · Cited by 113 · see citing works
Learning from bacterial competition in the host to develop antimicrobials
Raffatellu, M. (2018) · Nature Medicine · doi:10.1038/s41591-018-0145-0 · Cited by 110 · see citing works
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Iron Regulatory Proteins Mediate Host Resistance to Salmonella Infection
Nairz, M., Ferring-Appel, D., Casarrubea, D., Sonnweber, T., Viatte, L., Schroll, A., Haschka, D., Fang, F. C., Hentze, M. W., Weiss, G., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.06.017 · Cited by 103 · see citing works
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The Microbiota Shifts the Iron Sensing of Intestinal Cells
Deschemin, J., Noordine, M., Remot, A., Willemetz, A., Afif, C., Canonne‐Hergaux, F., Langella, P., Karim, Z., Vaulont, S., Thomas, M., et al. (2016) · The FASEB Journal · doi:10.1096/fj.15-276840 · Cited by 108 · see citing works
Salmonella enterica Serovar Typhimurium Strategies for Host Adaptation
Anderson, C. J., & Kendall, M. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01983 · Cited by 106 · see citing works
Deciphering the interplay between the genotoxic and probiotic activities of Escherichia coli Nissle 1917
Massip, C., Branchu, P., Bossuet‐Greif, N., Chagneau, C. V., Gaillard, D., Martín, P., Boury, M., Sécher, T., Dubois, D., Nougayrède, J., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1008029 · Cited by 105 · see citing works
Iron Supplements Modulate Colon Microbiota Composition and Potentiate the Protective Effects of Probiotics in Dextran Sodium Sulfate-induced Colitis
Constante, M., Fragoso, G., Lupien‐Meilleur, J., Calvé, A., & Santos, M. M. (2017) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000001089 · Cited by 107 · see citing works
Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut
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Host-Microbe Competition for Zinc in the Inflamed Gut
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Self-citation

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: Liu, Janet Z.
Pezeshki, Milad
Edwards, Robert A.
Contreras, Heidi
Libby, Stephen J.
Fang, Ferric C.
Raffatellu, Manuela
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2013-07
Volume: 14
Issue: 1
Pages: 26-37
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2013.06.007
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 381 d)
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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Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron

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