Nutritional immunity: transition metals at the pathogen–host interface

Hood, M. Indriati; Skaar, Eric P.

doi:10.1038/nrmicro2836

Cited by 1,535Trace Elements in HealthBacterial Genetics and BiotechnologyIron Metabolism and Disorders

Nutritional immunity: transition metals at the pathogen–host interface

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Hood, M. Indriati, Skaar, Eric P.·2012·Nature Reviews Microbiology

DOI 10.1038/nrmicro2836PMC PMC3875331

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Abstract

Transition metals occupy an essential niche in biological systems. Their electrostatic properties stabilize substrates or reaction intermediates in the active sites of enzymes, and their heightened reactivity is harnessed for catalysis. However, this heightened activity also renders transition metals toxic at high concentrations. Bacteria, like all living organisms, must regulate their intracellular levels of these elements to satisfy their physiological needs while avoiding harm. It is therefore not surprising that the host capitalizes on both the essentiality and toxicity of transition metals to defend against bacterial invaders. This Review discusses established and emerging paradigms in nutrient metal homeostasis at the pathogen-host interface.

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Haptoglobin and haemopexin rapidly bind hemoglobin and haem released from erythrocytes respectively for iron recycling and to possibly avoid toxicity posed by free haem.
“Haptoglobin and haemopexin rapidly bind hemoglobin and haem released from erythrocytes respectively for iron recycling and to possible avoid toxicity posed by free haem (Kumar and Bandyopadhyay, 2005; Hood and Skaar, 2012).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Hood and Skaar, 2012
The 'Host mechanisms for withholding iron' section (page not provided) says that haptoglobin and haemopexin rapidly bind haemoglobin and haem, respectively, when released from erythrocytes. It describes this binding as limiting bacterial access to iron, but does not state that its purposes are iron recycling or avoiding free-haem toxicity. (LLM, conf=0.89)
Experimental — accuracy not yet measured
Fe is a redox-active trace metal that has important roles in most biological systems, supporting vital processes such as DNA replication, transcription and central metabolism.
“Fe is a redox- active trace metal that has important roles in most biological systems, supporting vital processes such as DNA replication, transcription and central metabolism 9 .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [9]
The “Fe limitation: a universal strategy in innate defence” section explicitly says Fe supports DNA replication, transcription and central metabolism in bacteria. The broader claim that it supports those specific processes in most biological systems goes beyond what this passage states, although the opening passage describes Fe as a commonly used redox-active metal. (LLM, conf=0.85)
Experimental — accuracy not yet measured
During infection, host nutritional immunity sequesters nutrients including iron, causing S. aureus to experience Fe limitation.
“Due to host nutritional immunity and iron (Fe) sequestration, S. aureus experiences Fe limitation during infection.”
From The oxidative stress regulator, PerR, is required for staphyloferrin B-mediated iron acquisition in Staphylococcus aureus (2026) · cites this paper as [7]
In the human host, iron is a highly restricted nutrient.
“Although iron is abundant within the earth crust, in the human host, iron is a highly restricted nutrient (Frey and Reed, 2012; Hood and Skaar, 2012).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Hood and Skaar, 2012
The concerted action of host Fe-binding proteins renders host Fe pools largely inaccessible to bacteria that lack high-affinity Fe uptake pathways or systems.
“The concerted action of these proteins renders host Fe pools largely inaccessible to bacteria that lack highaffinity Fe uptake pathways or systems 9,12,14 .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [9]

Vertebrates have developed numerous strategies to starve bacteria of nutrient metals via a process termed nutritional immunity.
“Vertebrates have developed numerous strategies to starve bacteria of nutrient metals via a process termed nutritional immunity 6,9,10 .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [9]
The prominent strategies that bacteria use to acquire Fe include the secretion of siderophores and the uptake of siderophore-Fe, haem-Fe or kinetically labile ferrous Fe.
“The prominent strategies that bacteria use to acquire Fe include the secretion of siderophores and the uptake of siderophore-Fe, haem-Fe or kinetically labile ferrous Fe (ref. 9 ) .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [9]
This withholding of iron is an innate defense mechanism known as nutritional immunity.
“This is an innate defense mechanism known as ‘nutritional immunity’.101”
From Iron metabolism and iron disorders revisited in the hepcidin era (2020) · cites this paper as [101]
S100A8 and S100A9 form the heterodimeric complex calprotectin, which is mainly expressed by PMN.
“Two of these proteins, S100A8 and S100A9, form a heterodimeric complex named calprotectin and are mainly expressed by PMN.”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [233]
Bacterial periplasmic superoxide-dismutases contain zinc or manganese to elaborate defense against host-mediated oxidative stress, and bacteria have a need for these metals.
“Bacterial periplasmic superoxide-dismutases (SOD) contain zinc or manganese to elaborate their defense against host-mediated oxidative stress, and bacteria thus have a certain need for these metals (233).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [233]
Copper plays important roles as a prosthetic group for many enzymes such as cytochromes, proteins involved in oxidative phosphorylation, or copper/zinc-superoxide dismutase.
“In addition, copper plays important roles as a prostethic group for many enzymes such as cytochromes, proteins involved in oxidative phosphorylation or copper/zinc-superoxide dismutase (233).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [233]
S100 proteins can be induced by IL-17 and IL-22, exert pro-inflammatory activity, and may promote chemotaxis of PMN.
“In addition, S100 proteins can be induced by IL-17 and IL-22, and S100 proteins exert pro-inflammatory activity and may promote chemotaxis of PMN (233, 244).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [233]
Components of the S100 protein family bind Zn+2, Cu+2, and Mn+2, thereby exerting anti-microbial activity.
“Components of the S100 protein family bind Zn+2, Cu+2, and Mn+2, which thereby exert anti-microbial activity (233).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [233]
Iron restriction to the pathogen is a powerful innate immune defense mechanism of the host called nutritional immunity.
“Nutritional immunity, a strategy of the immune system to deprive essential nutrients, such as divalent metals including iron, from invading pathogens”
From Iron in immune cell function and host defense (2021) · cites this paper as [16]
Nutritional immunity has played a fundamental role in survival of primate populations challenged by microbes.
“Nutritional immunity, a strategy of the immune system to deprive essential nutrients, such as divalent metals including iron, from invading pathogens [16,17], has played a fundamental role in survival of primate populations challenged by microbes.”
From Iron in immune cell function and host defense (2021) · cites this paper as [16]
Host proteins that bind free iron prevent microbes from acquiring it, a protective effect named nutritional immunity.
“The sequestration of free iron by host proteins simultaneously prevents acquisition by microbes, a protective effect termed nutritional immunity (see Glossary) 5, 6.”
From Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy (2015) · cites this paper as [5]
Iron sequestration is a key innate immune defense called nutritional immunity.
“The sequestration of essential iron has emerged as a crucial innate defense system termed nutritional immunity”
From Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy (2015) · cites this paper as [5]
Nutritional immunity relies on the sequestration of essential molecules such as iron, preventing the growth of pathogens.
“An important host defense strategy against infection, known as “nutritional immunity,” relies on the sequestration of essential molecules, such as iron, preventing the growth of pathogens (2).”
From Iron- and Hepcidin-Independent Downregulation of the Iron Exporter Ferroportin in Macrophages during Salmonella Infection (2017) · cites this paper as [2]
Competition for limited iron became a conserved host defense against infection in plants and animals and also a microbial virulence factor.
“where competition for limited Fe resources emerged as an evolutionary conserved host defense strategy against infection in plants (2) and animals (3–5) as well as a microbial virulence factor (6).”
From Innate Nutritional Immunity (2018) · cites this paper as [4]
Most pathogens evolved ways to divert host iron into their own metabolism, while hosts evolved ways to restrict pathogen iron access.
“Presumably, this explains why most pathogens evolved a variety of strategies aimed at diverting Fe from their hosts into their own metabolic pathways, while hosts co-evolved strategies to restrict pathogens from accessing Fe (3–6).”
From Innate Nutritional Immunity (2018) · cites this paper as [4]
Nutritional immunity includes host manipulation of manganese, zinc, and other transition metals to starve or intoxicate pathogens.
“Nutritional immunity has since been expanded to include the host processes that manipulate local levels of manganese, zinc, and other transition metals in order to metal starve or intoxicate the invading pathogens”
From Heme Synthesis and Acquisition in Bacterial Pathogens (2016) · cites this paper as [16]
Limited pathogen access to metals is an antimicrobial strategy and limits bacterial replication.
“The limited access of pathogens to metals serves as an antimicrobial strategy and limits bacterial replication.”
From Heme Synthesis and Acquisition in Bacterial Pathogens (2016) · cites this paper as [16]
Host nutritional immunity restricts bacterial access to zinc, manganese, and nonmetal nutrients such as amino acids, in addition to iron.
“Thirty years later, Eugene Weinberg popularized the term nutritional immunity to describe the phenomenon, which has since been expanded to include host restriction of zinc, manganese, and nonmetal nutrients such as amino acids (65, 140, 149).”
From Transition Metals and Virulence in Bacteria (2016) · cites this paper as [65]
Conflict exists between hosts and invading pathogens over control of iron.
“Conflict exists between hosts and invading pathogens over the control of the critical micronutrient, iron (reviewed in [8,9]).”
From Rapidly Escalating Hepcidin and Associated Serum Iron Starvation Are Features of the Acute Response to Typhoid Infection in Humans (2015) · cites this paper as [9]
Iron and other components of nutritional immunity (e.g., zinc) regulate essential metabolic and inflammatory pathways in immune cells.
“iron and other components of nutritional immunity (e.g., zinc) regulate essential metabolic and inflammatory pathways in immune cells that are largely uncharacterized (365, 599).”
From Aspergillus fumigatus and Aspergillosis in 2019 (2019) · cites this paper as [365]
Most TFs are zinc-dependent proteins, and almost 50% of all eukaryotic enzymes are zinc-containing proteins.
“Most TFs are zinc-dependent proteins, and almost 50% of all eukaryotic enzymes are zinc-containing proteins (365).”
From Aspergillus fumigatus and Aspergillosis in 2019 (2019) · cites this paper as [365]
Iron and other components of nutritional immunity regulate essential metabolic and inflammatory pathways in immune cells that are largely uncharacterized.
“apart from inhibiting pathogen growth, iron and other components of nutritional immunity (e.g., zinc) regulate essential metabolic and inflammatory pathways in immune cells that are largely uncharacterized (365, 599).”
From Aspergillus fumigatus and Aspergillosis in 2019 (2019) · cites this paper as [365]

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[19]Ratcliff-Griffin M Wilks A Stojiljkovic I Iron transport in bacteria: molecular genetics, biochemistry, microbial pathogenesis and ecology Crosa JH Mey AR Payne SM 86 94 ASM Press Washington, D.C. 2004

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“…effect against such infections via acidification of the microbe containing phagosome, but also by altering the cellular distribution of divalent metals such as zinc, manganese or iron which all play decisive role in host–pathogen interaction (Hood and Skaar, 2012; Diaz-Ochoa et al., 2014).”
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Authors: Hood, M. I., & Skaar, E. P.
Affiliations: Vanderbilt University (US)
Corresponding author: Skaar, Eric P.
ORCID: Skaar, Eric P.
Venue: Nature Reviews Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2012-07-16
Volume: 10
Issue: 8
Pages: 525-537
ISSN: 1740-1526 (ISSN-L)
1740-1534
DOI: 10.1038/nrmicro2836
PMC: PMC3875331
OpenAlex: W1964339096
Cited by: 1,535
References: 154
Citations by year: 2026: 132 · 2025: 97 · 2024: 118 · 2023: 107 · 2022: 152 · 2021: 150 · 2020: 129 · 2019: 147 · 2018: 97 · 2017: 115 · 2016: 97 · 2015: 87 · 2014: 52 · 2013: 40 · 2012: 11
FWCI: 7.40
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature Reviews Microbiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health
National Institute of Allergy and Infectious Diseases (AI 069233, AI073843, AI091771, R01AI069233, R56AI091771, R01AI073843)
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Keywords: nutritional immunity, transition metals, metal homeostasis, host-pathogen arms race, metal sequestration, metal toxicity
MeSH terms: Bacteria, Food, Humans, Metals, Transition Elements, Host-Pathogen Interactions

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Nutritional immunity: transition metals at the pathogen–host interface

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