Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy

Barber, Matthew F.; Elde, Nels C.

doi:10.1016/j.tig.2015.09.001

Cited by 118Iron Metabolism and DisordersBacterial Genetics and BiotechnologyEvolution and Genetic Dynamics

Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy

Open access

Barber, Matthew F., Elde, Nels C.·2015·Trends in Genetics

DOI 10.1016/j.tig.2015.09.001PMC PMC4639441

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Abstract

Host-pathogen interactions provide valuable systems for the study of evolutionary genetics and natural selection. The sequestration of essential iron has emerged as a crucial innate defense system termed nutritional immunity, leading pathogens to evolve mechanisms of 'iron piracy' to scavenge this metal from host proteins. This battle for iron carries numerous consequences not only for host-pathogen evolution but also microbial community interactions. Here we highlight recent and potential future areas of investigation on the evolutionary implications of microbial iron piracy in relation to molecular arms races, host range, competition, and virulence. Applying evolutionary genetic approaches to the study of microbial iron acquisition could also provide new inroads for understanding and combating infectious disease.

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Written from the paper’s full text.

TL;DR

This review argues that host sequestration of iron—nutritional immunity—creates a selective arena in which microbes evolve “iron piracy” mechanisms, producing molecular arms races, host-range barriers, microbial competition, and virulence shifts. It synthesizes evolutionary and microbiological evidence to propose iron acquisition as a model for studying Red Queen and Black Queen dynamics in infection.

Key findings

Nutritional immunity depends on host iron-binding proteins such as transferrin, lactoferrin, hemoglobin, and lipocalin 2; microbes counter with siderophores, surface receptors for host proteins, heme acquisition, and ferric reductases.
Primate transferrin shows signatures of positive selection, and rapidly evolving sites overlap the binding interface with bacterial transferrin-binding protein A (TbpA); single amino acid changes can alter TbpA binding specificity, including for the human transferrin C2 variant, which some but not all pathogens recognize.
Iron piracy influences host range and disease: transferrin receptor specificity is linked to narrow host ranges, probiotic *E. coli* Nissle 1917 suppresses *Salmonella* through iron competition in a lipocalin 2-dependent manner, and *Pseudomonas aeruginosa* shows selected heme-uptake promoter changes after more than 36 years of persistent cystic fibrosis colonization.
The review connects iron to Red Queen arms races and Black Queen gene-loss dynamics, citing *Borrelia burgdorferi*’s loss of iron requirement and substitution of manganese, and notes that the hemochromatosis C282Y mutation is carried by roughly 10% of people of European descent and may involve infection-related trade-offs.

Methods

Narrative review and synthesis, not a primary experimental study; no systematic review or meta-analytic protocol is described.
Evidence comes from cited microbiological, genetic, phylogenetic, and evolutionary studies, including the authors’ prior work on transferrin–TbpA conflict.
Main analysis is conceptual integration of findings across host–pathogen interactions, microbial competition, host range, and virulence evolution.

Limitations

The paper states that many questions remain, including whether nutritional immunity factors beyond transferrin engage in arms races, whether manganese and zinc systems show similar conflicts, and how iron shapes cooperative microbial communities.
The authors note that the discussion focuses largely on bacteria, while fungi and parasites are also likely subject to comparable conflicts.
Evident from the text: as a narrative review, it does not provide new primary data, systematic search criteria, or quantitative synthesis, and several conclusions depend on cited studies rather than reanalysis.

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Integrity signals

Registry

Crossref · 10.1016/j.tig.2015.09.001

Cites

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Statistics

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Claims the paper makes

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Findingcitation
The authors' recent work identified iron competition as a new interface for Red Queen conflicts.
“Our recent work highlighted the battle for iron as a new interface for Red Queen evolutionary conflicts [36].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
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Findingown data
Rapidly evolving sites in primate transferrin almost completely overlap the TbpA binding interface.
“rapidly evolving sites almost entirely overlap with the binding interface of a bacterial surface receptor, transferrin-binding protein A (TbpA)”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
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Findingown data
Transferrin has undergone strong positive selection in primates.
“Not only has transferrin been subject to strong positive selection in primates”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
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Findingown data
Single amino acid changes at rapidly evolving transferrin sites can control TbpA binding specificity among related primates and for the human C2 variant.
“Single amino acid substitutions at rapidly evolving sites in transferrin were sufficient to control TbpA-binding specificities between related primates as well as for an abundant human transferrin variant, termed C2 (Figure 2B).”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
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Findingcitation
Single rapidly evolving transferrin sites can dictate TbpA-binding differences between humans and chimpanzees.
“Our recent work further demonstrated that single rapidly evolving sites in transferrin are sufficient to dictate TbpA-binding differences between even our closest relatives, such as chimpanzees [36].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
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Premisecitation
A common strategy is to secrete siderophores, small chelators whose iron affinity exceeds that of transferrin.
“One of the most common microbial iron acquisition strategies involves the secretion of siderophores, small molecule chelators, which possess an affinity for iron unmatched even by proteins such as transferrin 17, 18.”
Quote in the paperNot a substantial claim0 of 2 sources checked
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Premisecitation
Fungal pathogens use ferric reductases to convert transferrin- or lactoferrin-bound ferric iron into soluble ferrous iron.
“Ferric reductases are an important class of iron acquisition systems in fungal pathogens, which convert transferrin or lactoferrin-bound ferric iron into a soluble ferrous form [27].”
Quote in the paperNot a substantial claim0 of 1 sources checked
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Premisecitation
TbpA is an important virulence factor in several human and agricultural pathogens.
“transferrin-binding protein A (TbpA), an important virulence factor in several human pathogens including Neisseria meningitidis, Neisseria gonorrhoeae, Haemophilus influenzae, and Moraxella catarrhalis, as well as a number of agricultural pathogens (Figure 2A) 21, 37, 38, 39, 40, 41.”
Quote in the paperSubstantial claim0 of 6 sources checked
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- cites [39] Yu R.H. Schryvers A.B. The interaction between human transferrin and transferrin binding protein 2 from Moraxella (Branhamella) catarrhalis differs from that of other human pathogens Microb. Pathog. 15 1993 433 445 8007816 source
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- cites [41] Noinaj N. Structural basis for iron piracy by pathogenic Neisseria Nature 483 2012 53 58 22327295 PMC3292680 source
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Premisecitation
Schade and Caroline found that raw egg white strongly blocked growth of many bacteria and fungi.
“the researchers observed that addition of raw egg white to their culture media severely inhibited the growth of diverse bacteria as well as fungi.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [7] Schade A.L. Caroline L. Raw hen egg white and the role of iron in growth inhibition of Shigella dysenteriae, Staphylococcus aureus, Escherichia coli and Saccharomyces cerevisiae Science 100 1944 14 15 17783793 source
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Premisecitation
Some microbes have receptors that directly recognize and remove iron from transferrin and lactoferrin.
“several microbes also express receptors that directly recognize and extract iron from host proteins including transferrin and lactoferrin 19, 20, 21, 22, 23.”
Quote in the paperNot a substantial claim0 of 5 sources checked
- cites [19] Schryvers A.B. Morris L.J. Identification and characterization of the human lactoferrin-binding protein from Neisseria meningitidis Infect. Immun. 56 1988 1144 1149 3128478 PMC259775 source
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- cites [20] Lee B.C. Schryvers A.B. Specificity of the lactoferrin and transferrin receptors in Neisseria gonorrhoeae Mol. Microbiol. 2 1988 827 829 2850444 source
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- cites [21] Cornelissen C.N. Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors J. Bacteriol. 174 1992 5788 5797 1325963 PMC207106 source
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- cites [22] Salmon D. A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in T. brucei Cell 78 1994 75 86 8033214 source
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Premisecitation
Among 31 elements tested, only iron restored microbial growth in egg white.
“Of 31 individual elements tested, supplementation with iron alone was sufficient to restore microbial growth in the presence of egg white.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [7] Schade A.L. Caroline L. Raw hen egg white and the role of iron in growth inhibition of Shigella dysenteriae, Staphylococcus aureus, Escherichia coli and Saccharomyces cerevisiae Science 100 1944 14 15 17783793 source
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Premisecitation
Two years later, similar antimicrobial activity was detected in human blood serum.
“Two years later the scientists reported similar activity present in human blood serum [8].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [8] Schade A.L. Caroline L. An iron-binding component in human blood plasma Science 104 1946 340 341 17774530 source
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Premisecitation
The nutritional immunity theory accounted for the high susceptibility to bacterial and fungal infections seen in human iron overload disorders such as hereditary hemochromatosis and thalassemia.
“Weinberg's theory explained previous observations that human iron overload disorders such as hereditary hemochromatosis and thalassemia render affected individuals highly susceptible to bacterial and fungal infections.”
Quote in the paperNot a substantial claim
Premisecitation
Withholding nutrient iron is an alternative host defense against bacterial and eukaryotic pathogens.
“Nutrient iron sequestration provides one such alternative mode of host defense against bacteria and eukaryotic pathogens [3].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [3] Cassat J.E. Skaar E.P. Iron in infection and immunity Cell Host Microbe 13 2013 509 519 23684303 PMC3676888 source
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Premisecitation
Repeated positive selection at host-pathogen interfaces can create molecular arms races.
“Recurrent bouts of positive selection at such interfaces can give rise to so-called ‘molecular arms races’, in which the host and pathogen must continually adapt to maintain comparative fitness [1].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [1] Daugherty M.D. Malik H.S. Rules of engagement: molecular insights from host–virus arms races Annu. Rev. Genet. 46 2012 677 700 23145935 source
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Premisecitation
Infection causes an acute drop in circulating iron levels.
“George Cartwright's earlier observations that infection induces an acute reduction in circulating iron levels 12, 13, 14.”
Quote in the paperSubstantial claim0 of 3 sources checked
- cites [12] Weinberg E.D. Iron and infection Microbiol. Rev. 42 1978 45 66 379572 PMC281418 source
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Premisecitation
Later microbiology and molecular genetics showed nutritional immunity is pivotal against bacteria, fungi, and parasites.
“Subsequent microbiology and molecular genetic studies established that nutritional immunity plays a pivotal role in defense against an array of pathogens, including bacteria, fungi, and parasites 3, 15.”
Quote in the paperNot a substantial claim0 of 2 sources checked
- cites [3] Cassat J.E. Skaar E.P. Iron in infection and immunity Cell Host Microbe 13 2013 509 519 23684303 PMC3676888 source
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- cites [15] Skaar E.P. The battle for iron between bacterial pathogens and their vertebrate hosts PLoS Pathog. 6 2010 e1000949 20711357 PMC2920840 source
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Premisereasoning
Genes involved in such conflicts often have elevated dN/dS, indicating selection for amino acid changes at interaction surfaces.
“Genes subject to such evolutionary conflicts are often characterized by an increased rate of nonsynonymous to synonymous substitutions (termed dN/dS or ω), reflecting recurrent selection for novel amino acid substitutions that alter protein interaction surfaces.”
Quote in the paperNot a substantial claim
Premisereasoning
Free iron levels in circulation are far below the amounts microbes need for optimal growth.
“Owing to the iron-binding properties of proteins, such as transferrin, circulating levels of free iron in the body are orders of magnitude below the requirements for optimal microbial growth.”
Quote in the paperSubstantial claim
Premisecitation
Microbes respond to iron starvation by actively taking iron from host proteins.
“Microbes respond to iron starvation by actively scavenging this nutrient from host proteins to meet their metabolic requirements (Figure 1 ) [16].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [16] Ratledge C. Dover L.G. Iron metabolism in pathogenic bacteria Annu. Rev. Microbiol. 54 2000 881 941 11018148 source
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Premisecitation
Other microbes obtain heme from abundant host proteins such as hemoglobin.
“Additional mechanisms involve the acquisition of heme, the iron-containing porphyrin cofactor, from abundant host proteins such as hemoglobin 24, 25, 26.”
Quote in the paperNot a substantial claim0 of 3 sources checked
- cites [24] Lewis L.A. Dyer D.W. Identification of an iron-regulated outer membrane protein of Neisseria meningitidis involved in the utilization of hemoglobin complexed to haptoglobin J. Bacteriol. 177 1995 1299 1306 7868605 PMC176737 source
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- cites [26] Fabian M. Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the Gram-positive pathogen Bacillus anthracis J. Biol. Chem. 284 2009 32138 32146 19759022 PMC2797284 source
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Premisecitation
Pathogens have evolved ways to steal iron from host proteins.
“leading pathogens to evolve mechanisms of ‘iron piracy’ to scavenge this metal from host proteins”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [16] Ratledge C. Dover L.G. Iron metabolism in pathogenic bacteria Annu. Rev. Microbiol. 54 2000 881 941 11018148 source
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Interpretationcitation
Using genetic variants of transferrin in protein-based therapeutics offers a new way to treat infectious disease.
“Applying genetic variants of transferrin to protein-based therapeutics provides one new means of treating infectious disease [78].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [78] Lin L. Transferrin iron starvation therapy for lethal bacterial and fungal infections J. Infect. Dis. 210 2014 254 264 24446527 PMC4092247 source
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Premisecitation
The increased susceptibility to extracellular pathogens in hereditary hemochromatosis may be balanced by resistance to macrophage-infecting pathogens such as Mycobacterium tuberculosis and Salmonella Typhi.
“this increased susceptibility to extracellular pathogens may be offset by resistance to others that normally infect macrophages such as Mycobacterium tuberculosis or Salmonella enterica serovar Typhi, which cause tuberculosis and typhoid fever, respectively [65].”
Quote in the paperSubstantial claim0 of 1 sources checked
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Premisecitation
Pathogens with restricted host iron requirements, including N. gonorrhoeae and S. aureus, are urgent public health concerns because of rising antibiotic resistance.
“pathogens exhibiting restricted host iron requirements, including N. gonorrhoeae and S. aureus, pose urgent public health concerns given their increasing resistance to conventional antibiotics [77].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [77] Blair J.M.A. Molecular mechanisms of antibiotic resistance Nat. Rev. Microbiol. 13 2015 42 51 25435309 source
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Interpretationown data
Positive selection signatures at the transferrin-TbpA interface suggest this interaction was a key infection determinant over millions of years of primate divergence.
“Genetic signatures of positive selection at the transferrin–TbpA binding interface suggest that this interaction has been a key determinant of infection during millions of years of primate divergence.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
  Not checked in the free run.
Premisecitation
Lactoferrin has gained mutations that create antimicrobial peptide domains able to bind and disrupt pathogen membranes.
“in addition to sequestering iron, lactoferrin has acquired mutations to generate antimicrobial peptide (AMP) domains that bind and disrupt pathogen membranes 45, 46.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [45] Yamauchi K. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment Infect. Immun. 61 1993 719 728 8423097 PMC302785 source
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- cites [46] Haney E.F. Novel lactoferrampin antimicrobial peptides derived from human lactoferrin Biochimie 91 2009 141 154 18534196 source
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Premisecitation
People with hereditary hemochromatosis are highly susceptible to normally noninvasive microbes such as Vibrio vulnificus and Yersinia enterocolitica.
“individuals with HH are highly susceptible to infection by normally noninvasive microbes, such as the bacteria Vibrio vulnificus and Yersinia enterocolitica 62, 63, 64.”
Quote in the paperSubstantial claim0 of 3 sources checked
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- cites [63] Quenee L.E. Hereditary hemochromatosis restores the virulence of plague vaccine strains J. Infect. Dis. 206 2012 1050 1058 22896664 PMC3501692 source
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- cites [64] Weinberg E.D. Microbial pathogens with impaired ability to acquire host iron Biometals 13 2000 85 89 10831229 source
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Premisecitation
Lipocalin 2 is a potent innate immune factor that binds and sequesters siderophores, blocking microbial uptake.
“the vertebrate protein lipocalin 2 (also known as siderocalin or NGAL) is a potent innate immunity factor that functions in part through binding and sequestration of siderophores, preventing their uptake by microbes 50, 51.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [50] Flo T.H. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron Nature 432 2004 917 921 15531878 source
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- cites [51] Bachman M.A. Interaction of lipocalin 2, transferrin, and siderophores determines the replicative niche of Klebsiella pneumoniae during pneumonia MBio 3 2012 e00224 e311 23169997 PMC3509427 source
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Interpretationcitation
Transferrin variation likely affects host range beyond bacteria because transferrin receptors are involved in iron acquisition and tropism of Trypanosoma brucei.
“The implications for transferrin variation on host range likely extend beyond bacteria as well, given that transferrin receptors have been implicated in iron acquisition and tropism of Trypanosoma brucei, the eukaryotic parasite that causes African sleeping sickness 73, 74.”
Quote in the paperNot a substantial claim0 of 2 sources checked
- cites [73] Bitter W. The role of transferrin-receptor variation in the host range of Trypanosoma brucei Nature 491 1998 499 502 9461219 source
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- cites [74] Steverding D. The significance of transferrin receptor variation in Trypanosoma brucei Trends Parasitol. 19 2003 125 127 12643995 source
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Interpretationcitation
Several studies have linked nutritional immunity factors to restriction of bacterial host range.
“A number of studies have now implicated nutritional immunity factors in restricting the host range of several bacterial pathogens.”
Quote in the paperSubstantial claim
- Rests on an assumption: Bacteria that use transferrin receptors have extremely narrow host ranges.
Interpretationreasoning
Iron acquisition is a leaky process that may be especially prone to Black Queen conflicts.
“Iron acquisition is one such ‘leaky’ biological process that may be particularly prone to Black Queen conflicts.”
Quote in the paperSubstantial claim
Premisecitation
Borrelia burgdorferi does not require iron, unlike nearly all other organisms.
“the bacterial spirochete Borrelia burgdorferi, the causative agent of Lyme disease, lacks a requirement for iron shared by nearly all other organisms [54].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [54] Posey J.E. Gherardini F.C. Lack of a role for iron in the Lyme disease pathogen Science 288 2000 1651 1653 10834845 source
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Premisecitation
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].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [82] Deriu E. Probiotic bacteria reduce Salmonella typhimurium intestinal colonization by competing for iron Cell Host Microbe 14 2013 26 37 23870311 PMC3752295 source
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Premisecitation
Giving mice human transferrin can promote infection by human-specific Neisseria.
“expressing or injecting human transferrin in mice can promote infection with human-specific Neisseria 71, 72.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [71] Oftung F. A mouse model utilising human transferrin to study protection against Neisseria meningitidis serogroup B induced by outer membrane vesicle vaccination FEMS Immunol. Med. Microbiol. 26 1999 75 82 10518045 source
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- cites [72] Zarantonelli M.L. Transgenic mice expressing human transferrin as a model for meningococcal infection Infect. Immun. 75 2007 5609 5614 17893132 PMC2168318 source
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Premisecitation
Some pathogens avoid lipocalin 2 by making modified stealth siderophores that it does not recognize.
“Some pathogens evade this defense through production of modified ‘stealth siderophores’, which are not recognized by lipocalin 2 52, 53.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [52] Hantke K. Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN Proc. Natl. Acad. Sci. U.S.A. 100 2003 3677 3682 12655053 PMC152981 source
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- cites [53] Abergel R.J. Anthrax pathogen evades the mammalian immune system through stealth siderophore production Proc. Natl. Acad. Sci. U.S.A. 103 2006 18499 18503 17132740 PMC1693691 source
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Interpretationreasoning
Studies of hereditary hemochromatosis illustrate how iron's role in infection may contribute to antagonistic pleiotropy in human genetic disorders.
“these studies provide fascinating examples of how the role of iron in infection may contribute to instances of antagonistic pleiotropy in human genetic disorders.”
Quote in the paperSubstantial claim
- Rests on an assumption: The C282Y mutation in HFE causes hereditary hemochromatosis and is carried by roughly 10% of people of European descent.
- Rests on an assumption: HFE protein is expressed on cell surfaces and interacts with transferrin receptor to regulate gut iron absorption and macrophage iron release.
Interpretationnone given
Other nutritional immunity proteins probably help limit pathogen host range.
“In addition to transferrin, it is likely that other nutritional immunity proteins contribute to limiting pathogen host range.”
Quote in the paperNot a substantial claim
Interpretationreasoning
Adaptive evolution of nutritional immunity factors may be enough to create a host range barrier against pathogens.
“These findings suggest that adaptive evolution of nutritional immunity factors may be sufficient to establish a host range barrier against pathogens.”
Quote in the paperSubstantial claim
- Rests on an assumption: Bacteria that use transferrin receptors have extremely narrow host ranges.
Premisecitation
TbpA and TbpB recognize only their host's transferrin when tested against diverse mammals.
“TbpA and its coreceptor TbpB exclusively recognize their host transferrin proteins when compared with diverse mammals 68, 69, 70.”
Quote in the paperSubstantial claim0 of 3 sources checked
- cites [68] Schryvers A.B. Gonzalez G.C. Receptors for transferrin in pathogenic bacteria are specific for the host's protein Can. J. Microbiol. 36 1990 145 147 2110858 source
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- cites [69] Cornelissen C.N. Expression of gonococcal transferrin-binding protein 1 causes Escherichia coli to bind human transferrin J. Bacteriol. 175 1993 2448 2450 8468302 PMC204535 source
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- cites [70] Litt D.J. Neisseria meningitidis expressing transferrin binding proteins of Actinobacillus pleuropneumoniae can utilize porcine transferrin for growth Infect. Immun. 68 2000 550 557 10639416 PMC97175 source
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Interpretationreasoning
Nutritional immunity has strongly affected host fitness during human evolutionary history with microbes.
“More broadly, these results demonstrate that nutritional immunity, similar to more established immune pathways, has strongly impacted host fitness during our long and intertwined history with microbes.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [36] Barber M.F. Elde N.C. Escape from bacterial iron piracy through rapid evolution of transferrin Science 346 2014 1362 1366 25504720 PMC4455941 source
  Not checked in the free run.
Premisecitation
Many pathogens have receptors for other host iron-binding proteins, including lactoferrin.
“Many pathogens encode receptors for other host iron-binding proteins including lactoferrin, a transferrin paralog expressed in milk, saliva, tears, mucus, and the secondary granules of neutrophils 37, 42, 43, 44.”
Quote in the paperSubstantial claim0 of 4 sources checked
- cites [37] Schryvers A.B. Characterization of the human transferrin and lactoferrin receptors in Haemophilus influenzae Mol. Microbiol. 2 1988 467 472 2845224 source
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- cites [42] García-Montoya I.A. Lactoferrin a multiple bioactive protein: an overview Biochim. Biophys. Acta 1820 2012 226 236 21726601 PMC7127262 source
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- cites [43] Beddek A.J. Schryvers A.B. The lactoferrin receptor complex in Gram negative bacteria Biometals 23 2010 377 386 20155302 source
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- cites [44] Noinaj N. Structural insight into the lactoferrin receptors from pathogenic Neisseria J. Struct. Biol. 184 2013 83 92 23462098 PMC3716850 source
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Premisecitation
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.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [82] Deriu E. Probiotic bacteria reduce Salmonella typhimurium intestinal colonization by competing for iron Cell Host Microbe 14 2013 26 37 23870311 PMC3752295 source
  Not checked in the free run.
Premisecitation
Bacteria that do not make siderophores often have siderophore receptors, letting them use siderophores made by neighbors.
“It has been widely observed that bacteria that do not produce siderophores nonetheless express siderophore receptors, allowing them to harvest this resource at the expense of their neighbors [16].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [16] Ratledge C. Dover L.G. Iron metabolism in pathogenic bacteria Annu. Rev. Microbiol. 54 2000 881 941 11018148 source
  Not checked in the free run.
Premisecitation
Bacterial siderophore production follows many kin selection predictions, with relatedness and competition affecting emergence of non-producing cheaters.
“Previous studies have demonstrated that bacterial siderophore production follows many predictions of kin selection, whereby relatedness and degrees of competition influence the emergence of cheaters that do not produce siderophores 80, 81.”
Quote in the paperNot a substantial claim0 of 2 sources checked
- cites [80] Griffin A.S. Cooperation and competition in pathogenic bacteria Nature 430 2004 1024 1027 15329720 source
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- cites [81] Ghoul M. An experimental test of whether cheating is context dependent J. Evol. Biol. 27 2014 551 556 24480013 source
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Interpretationreasoning
Iron acquisition is a useful system for studying microbial population biology and evolution, including Black Queen dynamics.
“Iron acquisition therefore provides as an informative system in which to study microbial population biology and evolution, including Black Queen dynamics.”
Quote in the paperNot a substantial claim
Interpretationcitation
Other microbes probably have comparable regulatory networks.
“Given that iron starvation acts as a trigger for activation of virulence genes in many pathogens [92], it is likely that similar gene regulatory networks also exist in other microbes.”
Quote in the paperNot a substantial claim
Interpretationcitation
C. albicans has evolved a complex regulatory program for iron uptake that operates in both commensal and pathogenic states.
“Thus, C. albicans has evolved an intricate transcriptional program to regulate iron acquisition during commensal or pathogenic states [91].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [91] Noble S.M. Candida albicans specializations for iron homeostasis: from commensalism to virulence Curr. Opin. Microbiol. 16 2013 708 715 24121029 PMC3855070 source
  Not checked in the free run.
Premisecitation
Independent mutations in phu arose in P. aeruginosa from additional cystic fibrosis patients.
“Using experimental culture systems, the authors determined that increased expression of the phu system enhanced bacterial growth in a model of the CF lung, and that similar mutations had occurred independently in P. aeruginosa isolates from other patients with CF.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [88] Marvig R.L. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin MBio 5 2014 e00966 e1014 24803516 PMC4010824 source
  Not checked in the free run.
- Rests on an assumption: P. aeruginosa has several separate systems for acquiring iron, such as siderophores and heme uptake.
Interpretationreasoning
Commensal microbes could serve as a reservoir of virulence genes that pathogens can acquire.
“Commensal microbes may therefore provide a genetic stockpile of virulence factors available for acquisition by pathogens.”
Quote in the paperSubstantial claim
Interpretationreasoning
Both Red Queen and Black Queen processes appear to influence fundamental functions in microbial iron piracy.
“In the case of microbial iron piracy, both processes appear to play roles influencing fundamental functions.”
Quote in the paperSubstantial claim
Interpretationcitation
Greater heme uptake through hemoglobin likely helps P. aeruginosa move from an environmental organism to a specialized human pathogen.
“These results suggest that a shift to enhanced heme uptake via hemoglobin plays an important role in the transition of P. aeruginosa from an environmental microbe to a dedicated human pathogen.”
Quote in the paperSubstantial claim
- Rests on an assumption: P. aeruginosa has several separate systems for acquiring iron, such as siderophores and heme uptake.
Interpretationcitation
How a microbe acquires iron can determine whether it behaves as a commensal or a pathogen under changing conditions.
“Iron acquisition can also dictate the ability of a microbe to shift between commensalism and virulence as conditions change, as was recently observed in the yeast Candida albicans.”
Quote in the paperSubstantial claim
Interpretationreasoning
Dependence on these receptors creates Red Queen conflicts with host proteins such as transferrin, which contributes to the narrow host ranges of these strains.
“In turn, dependence on these receptors gives rise to Red Queen conflicts with host proteins, such as transferrin, contributing to narrow host ranges observed for these strains.”
Quote in the paperSubstantial claim
- Rests on an assumption: Bacteria that use transferrin receptors have extremely narrow host ranges.
Premisecitation
In pathogenic N. meningitidis and N. gonorrhoeae, transferrin receptors are key virulence factors.
“For example, while transferrin receptors are important virulence factors in pathogenic N. meningitidis and N. gonorrhoeae, these genes are also harbored by commensal Neisseria that inhabit the nasopharynx [93].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [93] Marri P.R. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species PLoS ONE 5 2010 e11835 20676376 PMC2911385 source
  Not checked in the free run.
Premisecitation
Boosting phu expression improved bacterial growth in a cystic fibrosis lung model.
“Using experimental culture systems, the authors determined that increased expression of the phu system enhanced bacterial growth in a model of the CF lung, and that similar mutations had occurred independently in P. aeruginosa isolates from other patients with CF.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [88] Marvig R.L. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin MBio 5 2014 e00966 e1014 24803516 PMC4010824 source
  Not checked in the free run.
- Rests on an assumption: P. aeruginosa has several separate systems for acquiring iron, such as siderophores and heme uptake.
Premisecitation
The Red Queen and Black Queen Hypotheses describe distinct evolutionary modes, from antagonistic arms races to adaptive gene loss.
“The Red Queen and Black Queen Hypotheses highlight distinct modes of evolutionary adaptation ranging from antagonistic arms races to adaptive gene loss [85].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [85] Morris J.J. Black Queen evolution: the role of leakiness in structuring microbial communities Trends Genet. 31 2015 475 482 26078099 source
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Premisecitation
Transferrin receptor genes are also found in commensal Neisseria living in the nasopharynx.
“For example, while transferrin receptors are important virulence factors in pathogenic N. meningitidis and N. gonorrhoeae, these genes are also harbored by commensal Neisseria that inhabit the nasopharynx [93].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [93] Marri P.R. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species PLoS ONE 5 2010 e11835 20676376 PMC2911385 source
  Not checked in the free run.
Premisecitation
In many pathogens, iron limitation triggers virulence gene expression.
“Given that iron starvation acts as a trigger for activation of virulence genes in many pathogens [92], it is likely that similar gene regulatory networks also exist in other microbes.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [92] Troxell B. Hassan H.M. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria Front. Cell Infect. Microbiol. 3 2013 59 24106689 PMC3788343 source
  Not checked in the free run.
Interpretationreasoning
Iron availability can shape evolutionary shifts between commensal and disease-causing microbial lifestyles.
“In addition to influencing interactions between microbes, iron can also regulate evolutionary transitions between commensal and pathogenic states.”
Quote in the paperSubstantial claim
Premisecitation
In P. aeruginosa strains persistently colonizing humans for more than 36 years, the promoter of phu, a heme uptake system, showed signs of positive selection.
“Among several potential adaptations that took place during this period, evidence of positive selection was detected in the promoter of phu, the bacterial heme uptake system.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [88] Marvig R.L. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin MBio 5 2014 e00966 e1014 24803516 PMC4010824 source
  Not checked in the free run.
- Rests on an assumption: P. aeruginosa has several separate systems for acquiring iron, such as siderophores and heme uptake.
Premisecitation
Sef1 and the repressor Sfu1 regulate each other.
“In addition, Sef1 is regulated by and itself regulates Sfu1, a transcriptional repressor.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [90] Chen C. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis Cell Host Microbe 10 2011 118 135 21843869 PMC3165008 source
  Not checked in the free run.
Interpretationreasoning
The Black Queen Hypothesis may explain the fitness advantage of bacterial receptors such as TbpA.
“The Black Queen Hypothesis may also provide a basis for understanding the fitness advantage conferred by bacterial receptors such as TbpA.”
Quote in the paperNot a substantial claim

Classified as probably not a substantial claim. 10
May combine two claims. 20

Classified as probably not a substantial claim.
Premisecitation
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.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [5] Hood M.I. Skaar E.P. Nutritional immunity: transition metals at the pathogen–host interface Nat. Rev. Microbiol. 10 2012 525 537 22796883 PMC3875331 source
  Not checked in the free run.
- cites [6] Potrykus J. Conflicting interests in the pathogen–host tug of war: fungal micronutrient scavenging versus mammalian nutritional immunity PLoS Pathog. 10 2014 e1003910 24626223 PMC3953404 source
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Classified as probably not a substantial claim.
Premisenone given
Iron is needed by microbes and hosts because it can switch between ferrous and ferric forms for redox reactions and electron transport.
“Iron is an essential micronutrient for microbes, as well as their hosts, due to its ability to readily shift between ferrous (Fe2+) and ferric (Fe3+) oxidative states for redox catalysis or electron transport.”
Quote in the paperSubstantial claim
May combine two claims.
Premisecitation
Several core vertebrate immune components engage in such conflicts, and some determine infection outcome.
“Several core components of the vertebrate immune system have subsequently been shown to engage in such conflicts, some of which are able to dictate the outcome of an infection 29, 30, 31, 32, 33, 34, 35.”
Quote in the paperNot a substantial claim0 of 7 sources checked
- cites [29] Sawyer S.L. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G PLoS Biol. 2 2004 e275 15269786 PMC479043 source
  Not checked in the free run.
- cites [30] Sawyer S.L. Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain Proc. Natl. Acad. Sci. U.S.A. 102 2005 2832 2837 15689398 PMC549489 source
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- cites [31] Elde N.C. Protein kinase R reveals an evolutionary model for defeating viral mimicry Nature 457 2008 485 489 19043403 PMC2629804 source
  Not checked in the free run.
- cites [32] Mitchell P.S. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA Cell Host Microbe 12 2012 598 604 23084925 PMC3540999 source
  Not checked in the free run.
- cites [33] Patel M.R. Convergent evolution of escape from hepaciviral antagonism in primates PLoS Biol. 10 2012 e1001282 22427742 PMC3302847 source
  Not checked in the free run.
- cites [34] Demogines A. Dual host–virus arms races shape an essential housekeeping protein PLoS Biol. 11 2013 e1001571 23723737 PMC3665890 source
  Not checked in the free run.
- cites [35] Sironi M. Evolutionary insights into host–pathogen interactions from mammalian sequence data Nat. Rev. Genet. 16 2015 224 236 25783448 PMC7096838 source
  Not checked in the free run.
May combine two claims.
Interpretationreasoning
Iron acquisition genes are virulence factors, which highlights iron's role in infection and the potential for evolutionary conflict.
“The identification of iron acquisition genes as pathogen virulence factors further underscores the role of iron in infection, as well as the potential for evolutionary conflicts to arise in the struggle for this precious nutrient.”
Quote in the paperSubstantial claim
Classified as probably not a substantial claim.
Premisecitation
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”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [5] Hood M.I. Skaar E.P. Nutritional immunity: transition metals at the pathogen–host interface Nat. Rev. Microbiol. 10 2012 525 537 22796883 PMC3875331 source
  Not checked in the free run.
- cites [6] Potrykus J. Conflicting interests in the pathogen–host tug of war: fungal micronutrient scavenging versus mammalian nutritional immunity PLoS Pathog. 10 2014 e1003910 24626223 PMC3953404 source
  Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation
The Red Queen Hypothesis proposes that antagonistic coevolution causes continual adaptation without permanent advantage.
“Leigh Van Valen's Red Queen Hypothesis, which proposed that antagonistic coevolution leads to a perpetual cycle of adaptation in which neither opponent gains a permanent advantage [28].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [28] Van Valen L. A new evolutionary law Evol. Theory 1 1973 1 30
  Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation
Weinberg proposed that depriving pathogens of iron is a cornerstone of host defense, which he called nutritional immunity.
“Eugene Weinberg proposed that withholding iron from microbial pathogens provided an important cornerstone of host defense, which he termed nutritional immunity [11].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [11] Weinberg E.D. Nutritional immunity. Host's attempt to withhold iron from microbial invaders JAMA 231 1975 39 41 1243565 source
  Not checked in the free run.
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Premisecitation
Transferrin is the protein responsible for this iron-binding activity and is central to animal iron metabolism.
“The factor responsible for this activity in both cases was later revealed to be the protein transferrin, which plays a central role in animal iron metabolism by binding and transporting this metal to target cells 9, 10.”
Quote in the paperNot a substantial claim0 of 2 sources checked
- cites [9] Ganz T. Nemeth E. Hepcidin and disorders of iron metabolism Annu. Rev. Med. 62 2011 347 360 20887198 source
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- cites [10] Gkouvatsos K. Regulation of iron transport and the role of transferrin Biochim. Biophys. Acta 1820 2012 188 202 22085723 source
  Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Premisecitation
Hereditary hemochromatosis involves increased gut iron absorption and serum iron overload, causing organ iron accumulation and tissue damage.
“Hereditary hemochromatosis (HH) is a condition characterized by increased iron absorption in the gut as well as serum iron overload, leading to iron accumulation in various organs and subsequent tissue damage 9, 60.”
Quote in the paperNot a substantial claim0 of 2 sources checked
- cites [9] Ganz T. Nemeth E. Hepcidin and disorders of iron metabolism Annu. Rev. Med. 62 2011 347 360 20887198 source
  Not checked in the free run.
- cites [60] Vujić M. Molecular basis of HFE-hemochromatosis Front. Pharmacol. 5 2014 42 24653703 PMC3949417
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May combine two claims.
Premisecitation
The B. burgdorferi genome has lost many iron-binding protein genes, and remaining iron-binding enzymes have been modified to use manganese.
“Closer inspection of the B. burgdorferi genome revealed that numerous genes encoding iron-binding proteins have been lost, and remaining enzymes that normally bind iron have undergone modification to bind manganese in its place 54, 55.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [54] Posey J.E. Gherardini F.C. Lack of a role for iron in the Lyme disease pathogen Science 288 2000 1651 1653 10834845 source
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- cites [55] Aguirre J.D. A manganese-rich environment supports superoxide dismutase activity in a Lyme disease pathogen, Borrelia burgdorferi J. Biol. Chem. 288 2013 8468 8478 23376276 PMC3605662 source
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Premisecitation
Hemoglobin mutations in sickle cell anemia give malaria resistance but cause severe anemia in homozygotes.
“Sickle cell anemia in humans provides a quintessential example, whereby hemoglobin mutations confer resistance to malaria infection at the expense of severe anemia in homozygous carriers [59].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [59] Ashley-Koch A. Sickle hemoglobin (HbS) allele and sickle cell disease: a HuGE review Am. J. Epidemiol. 151 2000 839 845 10791557 source
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Premisecitation
Staphylococcus aureus strongly prefers human hemoglobin over mouse hemoglobin, and this preference correlates with growth in murine infection models.
“Elegant work by Pishchany et al. demonstrated that the Gram-positive bacterium Staphylococcus aureus exhibits strong preference for human hemoglobin over mouse hemoglobin, which correlates with bacterial growth in murine models of infection [75].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [75] Pishchany G. Specificity for human hemoglobin enhances Staphylococcus aureus infection Cell Host Microbe 8 2010 544 550 21147468 PMC3032424 source
  Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Premisecitation
E. coli Nissle 1917 came from a WWI soldier who seemed resistant to dysentery and has been used as a probiotic for gastrointestinal ailments including ulcerative colitis and Crohn's disease.
“The Nissle 1917 strain of E. coli was isolated from a soldier during World War I who appeared resistant to an outbreak of dysentery, and has subsequently been applied as a probiotic treatment for gastrointestinal ailments including ulcerative colitis and Crohn's disease 83, 84.”
Quote in the paperNot a substantial claim0 of 2 sources checked
- cites [83] Nissle A. [Explanations of the significance of colonic dysbacteria and the mechanism of action of E. coli therapy (mutaflor)] Medizinische 4 1959 1017 1022 (in German) 13673841
  Not checked in the free run.
- cites [84] Jacobi C.A. Malfertheiner P. Escherichia coli Nissle 1917 (Mutaflor): new insights into an old probiotic bacterium Dig. Dis. 29 2011 600 607 22179217 source
  Not checked in the free run.
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Premisecitation
Many pathogens produce factors that either take lactoferrin-bound iron or block lactoferrin AMP activity.
“Many pathogens in turn encode factors that either scavenge lactoferrin-bound iron or inhibit associated AMP activity 47, 48, 49.”
Quote in the paperSubstantial claim0 of 3 sources checked
- cites [47] Hammerschmidt S. Identification of pneumococcal surface protein A as a lactoferrin-binding protein of Streptococcus pneumoniae Infect. Immun. 67 1999 1683 1687 10085004 PMC96514 source
  Not checked in the free run.
- cites [48] Senkovich O. Structure of a complex of human lactoferrin N-lobe with pneumococcal surface protein A provides insight into microbial defense mechanism J. Mol. Biol. 370 2007 701 713 17543335 PMC5356469 source
  Not checked in the free run.
- cites [49] Deka R.K. Crystal structure of the Tp34 (TP0971) lipoprotein of Treponema pallidum: implications of its metal-bound state and affinity for human lactoferrin J. Biol. Chem. 282 2007 5944 5958 17192261 source
  Not checked in the free run.
Classified as probably not a substantial claim.
Interpretationreasoning
Because nutritional immunity proteins also have core metal metabolism roles, arms races with pathogens could produce antagonistic pleiotropy that harms the host.
“Because many host nutritional immunity proteins also carry out crucial ‘day jobs’ in metal metabolism or transport, it is conceivable that antagonistic pleiotropy, or an evolutionary trade-off, could arise from an arms race with adverse consequences for the host.”
Quote in the paperSubstantial claim
Probably not a substantial claim: may not pass S3 (load-bearing).
Interpretationcitation
Fungi and parasites likely experience comparable evolutionary conflicts over iron.
“Finally, we have focused largely here on the role of bacteria in the evolutionary battle for iron, while fungi and parasites are undoubtedly also subject to similar conflicts 74, 99, 100.”
Quote in the paperNot a substantial claim0 of 3 sources checked
- cites [74] Steverding D. The significance of transferrin receptor variation in Trypanosoma brucei Trends Parasitol. 19 2003 125 127 12643995 source
  Not checked in the free run.
- cites [99] Kronstad J.W. An encapsulation of iron homeostasis and virulence in Cryptococcus neoformans Trends Microbiol. 21 2013 457 465 23810126 PMC3769505 source
  Not checked in the free run.
- cites [100] Jung W.H. Do E. Iron acquisition in the human fungal pathogen Cryptococcus neoformans Curr. Opin. Microbiol. 16 2013 686 691 23927895 source
  Not checked in the free run.
May combine two claims.
Premisecitation
C. albicans commonly lives as a gut commensal but can also grow in blood and cause systemic infection in vulnerable people.
“While often present as a commensal member of the gut microbiota, C. albicans is also capable of proliferating in the bloodstream and causing systemic infections in susceptible individuals [89].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [89] Cheng S-C. Interplay between Candida albicans and the mammalian innate host defense Infect. Immun. 80 2012 1304 1313 22252867 PMC3318407 source
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Premisecitation
Neisseria can take up DNA naturally, and gene transfer between pathogenic and commensal strains is common.
“Adding to this complexity, Neisseria are naturally competent and horizontal gene transfer readily occurs between pathogenic and commensal strains [94].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [94] Rotman E. Seifert H.S. The genetics of Neisseria species Annu. Rev. Genet. 48 2014 405 431 25251852 source
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Premisecitation
P. aeruginosa is common in the environment and usually does not cause disease in people with intact immunity.
“While P. aeruginosa is commonly found in the environment and is typically avirulent in immune-competent individuals, it readily colonizes the lungs of patients with cystic fibrosis (CF) where it poses a major source of mortality [87].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [87] Gellatly S.L. Hancock R.E.W. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses Pathog. Dis. 67 2013 159 173 23620179 source
  Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Premisecitation
P. aeruginosa colonizes cystic fibrosis lungs readily and is a major cause of death in those patients.
“While P. aeruginosa is commonly found in the environment and is typically avirulent in immune-competent individuals, it readily colonizes the lungs of patients with cystic fibrosis (CF) where it poses a major source of mortality [87].”
Quote in the paperNot a substantial claim0 of 1 sources checked
- cites [87] Gellatly S.L. Hancock R.E.W. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses Pathog. Dis. 67 2013 159 173 23620179 source
  Not checked in the free run.
May combine two claims.
Premisecitation
Chen et al. studied how a transcriptional network in C. albicans evolved, with Sef1 joining an existing iron-responsive repressor system to control growth in distinct host niches.
“Chen et al. dissected the evolution of an elaborate transcriptional network in C. albicans whereby incorporation of a novel transcriptional activator, Sef1, into a pre-existing iron-responsive repressor system mediates growth in different host niches [90].”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [90] Chen C. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis Cell Host Microbe 10 2011 118 135 21843869 PMC3165008 source
  Not checked in the free run.
May combine two claims.
Premisecitation
Sfu1 blocks iron uptake and is not needed for virulence, yet it is required for commensal growth in the gut.
“Sfu1 in turn represses iron acquisition and is dispensable for virulence, but is conversely essential for commensal growth in the gastrointestinal tract.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [90] Chen C. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis Cell Host Microbe 10 2011 118 135 21843869 PMC3165008 source
  Not checked in the free run.
May combine two claims.
Premisecitation
Genes for acquiring iron are recognized virulence factors; their loss reduces pathogenicity without killing the organism.
“Iron acquisition genes are now established as microbial virulence factors, in the sense that loss of these genes impairs pathogenicity without completely compromising organism viability 3, 86.”
Quote in the paperSubstantial claim0 of 2 sources checked
- cites [3] Cassat J.E. Skaar E.P. Iron in infection and immunity Cell Host Microbe 13 2013 509 519 23684303 PMC3676888 source
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- cites [86] Subashchandrabose S. Mobley H.L.T. Back to the metal age: battle for metals at the host–pathogen interface during urinary tract infection Metallomics 7 2015 935 942 25677827 PMC4634365 source
  Not checked in the free run.
May combine two claims.
Interpretationreasoning
Iron acquisition gene loss in B. burgdorferi can be seen as a Black Queen process inside host cells, while rapid evolution of bacterial transferrin receptors is a Red Queen conflict.
“loss of iron acquisition genes in B. burgdorferi could be interpreted as a Black Queen process arising within the host cell, whereas rapid evolution of bacterial transferrin receptors reflects a prototypical Red Queen conflict.”
Quote in the paperSubstantial claim
May combine two claims.
Premisecitation
Sef1 supports iron uptake and is required for virulence in living hosts.
“The authors demonstrated that Sef1 promotes iron acquisition and is essential for virulence in vivo.”
Quote in the paperSubstantial claim0 of 1 sources checked
- cites [90] Chen C. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis Cell Host Microbe 10 2011 118 135 21843869 PMC3165008 source
  Not checked in the free run.
May combine two claims.
Interpretationcitation
These findings show that microbial Black Queen dynamics can affect human disease and that beneficial microbes might be used to fight pathogens through iron sequestration.
“These findings further illustrate how microbial Black Queen dynamics can impact human disease, as well as the potential application of beneficial microbes to combat pathogens through iron sequestration.”
Quote in the paperSubstantial claim
May combine two claims.
Interpretationreasoning
By not making siderophores and instead targeting host iron-binding proteins, these bacteria use a less leaky system that may resist cheaters.
“By forgoing siderophore production and targeting host iron-binding proteins directly, these bacteria use a less leaky system, which may be inherently resistant to cheaters.”
Quote in the paperSubstantial claim

27 of 27

The paper relies on this without support.
The C282Y mutation in HFE causes hereditary hemochromatosis and is carried by roughly 10% of people of European descent.
“HH caused by the C282Y mutation in the HFE gene is the most common genetic disorder among those of European descent, carried by approximately 10% of these individuals.”
The paper relies on this without support.
HFE protein is expressed on cell surfaces and interacts with transferrin receptor to regulate gut iron absorption and macrophage iron release.
“HFE is expressed on the surface of several cell types where it interacts with the transferrin receptor Tf-R to regulate iron absorption in the gut and release of iron stored in circulating macrophages.”
The paper relies on this without support.
Bacteria that use transferrin receptors have extremely narrow host ranges.
“bacteria that utilize transferrin receptors possess extremely narrow host ranges, such as the human-specific N. gonorrhoeae and the porcine pathogen Actinobacillus pleuropneumoniae.”
The paper relies on this without support.
Most commensal microbes need iron to live yet seldom cause illness.
“In nearly all cases these organisms require iron for survival, and yet rarely if ever cause disease.”
The paper relies on this without support.
P. aeruginosa has several separate systems for acquiring iron, such as siderophores and heme uptake.
“P. aeruginosa, like many microbes, possesses multiple distinct iron acquisition systems, including siderophores and a heme uptake system.”

5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Both pathogens and the host have developed precise mechanisms that regulate iron uptake, utilization, and storage to prevent the threat posed by ROS.
“Both pathogens and the host have developed precise mechanisms that regulate iron uptake, utilization, and storage to prevent the threat posed by ROS (Barber and Elde, 2015).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Barber and Elde, 2015
In “An Evolving View of Host–Microbe Interactions” (page not provided), the paper says metazoans need coordinated iron transport and storage to prevent toxic free radicals. “The Battle for Iron” describes microbial iron-acquisition mechanisms, but does not say pathogens regulate iron uptake, utilization, and storage to prevent ROS damage. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Pathogenic microbes have evolved specialized mechanisms for obtaining iron from the host during infections, a process called iron piracy.
“Pathogenic microbes have evolved specialized mechanisms for obtaining iron from the host during infections (”
From Iron and infection (2018) · cites this paper as [5]
Co-evolution of humans and pathogens has produced an evolutionary arms race in nutritional immunity.
“suggesting that the co-evolution of humans and pathogens has produced an evolutionary arms race in the context of nutritional immunity [217,218].”
From Heme Synthesis and Acquisition in Bacterial Pathogens (2016) · cites this paper as [218]
Human and primate transferrin has undergone positive selection at the interface of binding by bacterial transferrin receptors.
“the human and primate iron-binding protein transferrin has undergone positive selection at the interface of binding by bacterial transferrin receptors”
From Heme Synthesis and Acquisition in Bacterial Pathogens (2016) · cites this paper as [218]

Molecular mechanisms of antibiotic resistance
Blair, J. M. A., Webber, M. A., Baylay, A. J., Ogbolu, D. O., & Piddock, L. J. V. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3380 · Cited by 4,092 · see citing works
A NEW EVOLUTIONARY LAW.
Valen, L. V. (1973) · Medical Entomology and Zoology · Cited by 2,468 · see citing works
Disorders of Iron Metabolism
Andrews, N. C. (1999) · New England Journal of Medicine · doi:10.1056/nejm199912233412607 · Cited by 2,130 · see citing works
Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron
Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., & Aderem, A. (2004) · Nature · doi:10.1038/nature03104 · Cited by 1,877 · see citing works
Iron Metabolism in Pathogenic Bacteria
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“Finally, we have focused largely here on the role of bacteria in the evolutionary battle for iron, while fungi and parasites are undoubtedly also subject to similar conflicts [74,99,100].”
Background
[Explanations of the significance of colonic dysbacteria & the mechanism of action of E. coli therapy (mutaflor)].
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Maize-soybean relay strip intercropping reshapes the rhizosphere bacterial community and recruits beneficial bacteria to suppress Fusarium root rot of soybean
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Metagenome to phenome approach enables isolation and genomics characterization of Kalamiella piersonii gen. nov., sp. nov. from the International Space Station
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Regulation of the Synthesis and Secretion of the Iron Chelator Cyclodipeptide Pulcherriminic Acid in Bacillus licheniformis
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A Key Role for the Periplasmic PfeE Esterase in Iron Acquisition via the Siderophore Enterobactin in Pseudomonas aeruginosa
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DGAT1 activity synchronises with mitophagy to protect cells from metabolic rewiring by iron depletion
Long, M., Sánchez-Martínez, Á., Longo, M., Suomi, F., Stenlund, H. C., Johansson, A. I., Ehsan, H., Salo, V. T., Montava‐Garriga, L., Naddafi, S., et al. (2022) · The EMBO Journal · doi:10.15252/embj.2021109390 · Cited by 46 · see citing works
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Nocardamine-Dependent Iron Uptake in Pseudomonas aeruginosa : Exclusive Involvement of the FoxA Outer Membrane Transporter
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FusC, a member of the M16 protease family acquired by bacteria for iron piracy against plants
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Low transferrin levels predict heightened inflammation in patients with COVID-19: New insights
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Scavenging Bacterial Siderophores with Engineered Lipocalin Proteins as an Alternative Antimicrobial Strategy
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Prevalence of virulence factor, antibiotic resistance, and serotype genes of Pasteurella multocida strains isolated from pigs in Vietnam
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Moonlighting of Haemophilus influenzae heme acquisition systems contributes to the host airway-pathogen interplay in a coordinated manner
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Habitat Adaptation Drives Speciation of a Streptomyces Species with Distinct Habitats and Disparate Geographic Origins
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Systematic identification of molecular mediators of interspecies sensing in a community of two frequently coinfecting bacterial pathogens
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Host–Pathogen Interactions of Marine Gram-Positive Bacteria
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Phenotypic Adaptation of Pseudomonas aeruginosa in the Presence of Siderophore-Antibiotic Conjugates during Epithelial Cell Infection
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Metschnikowia citriensis FL01 antagonize Geotrichum citri-aurantii in citrus fruit through key action of iron depletion
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Post-Translational Protein Deimination Signatures in Serum and Serum-Extracellular Vesicles of Bos taurus Reveal Immune, Anti-Pathogenic, Anti-Viral, Metabolic and Cancer-Related Pathways for Deimination
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Selective biotic stressors’ action on seed germination: A review
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Immune Cells and Microbiota Response to Iron Starvation
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Protease-associated import systems are widespread in Gram-negative bacteria
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Microbial siderophores for One Health
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Characterization of rhizosphere Pseudomonas chlororaphis IRHB3 in the reduction of Fusarium root rot and promotion of soybean growth
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New Shuttle Vectors for Real-Time Gene Expression Analysis in Multidrug-Resistant Acinetobacter Species: In Vitro and In Vivo Responses to Environmental Stressors
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Iron Acquisition and Metabolism as a Promising Target for Antimicrobials (Bottlenecks and Opportunities): Where Do We Stand?
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Whole genome sequencing of Moraxella bovis strains from North America reveals two genotypes with different genetic determinants
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Multi-faceted approaches to discovering and predicting microbial nutritional interactions
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Comparative Genomics, Siderophore Production, and Iron Scavenging Potential of Root Zone Soil Bacteria Isolated from ‘Concord’ Grape Vineyards
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Too much of a good thing
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Bioactive Compounds from and against Yeasts in the One Health Context: A Comprehensive Review
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Siderophore-mediated iron partition promotes dynamical coexistence between cooperators and cheaters
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Battle for Metals: Regulatory RNAs at the Front Line
Charbonnier, M., González-Espinoza, G., Kehl‐Fie, T. E., & Lalaouna, D. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.952948 · Cited by 19 · see citing works
Iron binding and release properties of transferrin-1 from Drosophila melanogaster and Manduca sexta: Implications for insect iron homeostasis
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Widespread fungal–bacterial competition for magnesium lowers bacterial susceptibility to polymyxin antibiotics
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No effect of intraspecific relatedness on public goods cooperation in a complex community
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How the Presence of Hemin Affects the Expression of the Different Iron Uptake Pathways in Pseudomonas aeruginosa Cells
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Microbial experimental evolution in a massively multiplexed and high-throughput era
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COVID-19 compromises iron homeostasis: Transferrin as a target of investigation
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Retinal ferroptosis as a critical mechanism for the induction of retinochoroiditis during ocular toxoplasmosis
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INTERGROWTH-21 Identifies High Prevalence of Low Symphysis–Fundal Height in Indigenous Pregnant Women Experiencing Multiple Infections, Nutrient Deficiencies, and Inflammation: The Maternal Infections, Nutrient Deficiencies, and Inflammation (MINDI) Cohort
González‐Fernández, D., Nemeth, E., Pons, E. D. C., Rueda, D., Sinisterra, O. T., Murillo, E., Sangkhae, V., Starr, L. M., Scott, M. E., & Koski, K. G. (2021) · Current Developments in Nutrition · doi:10.1093/cdn/nzab012 · Cited by 13 · see citing works
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Ecological selection of siderophore-producing microbial taxa in response to heavy metal contaminationPreprint
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The oxidative stress response of Francisella tularensis
Honn, M. (2016) · DiVA at Umeå University (Umeå University)

Authors: Barber, M. F., & Elde, N. C.
Affiliations: University of Utah (US)
Corresponding author: Barber, Matthew F.
ORCID: Barber, Matthew F.
Elde, Nels C.
Venue: Trends in Genetics
Publisher: Elsevier BV
Published: 2015-11
Volume: 31
Issue: 11
Pages: 627-636
ISSN: 0168-9525 (ISSN-L)
DOI: 10.1016/j.tig.2015.09.001
PMC: PMC4639441
OpenAlex: W2133773386
Cited by: 118
References: 104
Citations by year: 2026: 9 · 2025: 8 · 2024: 5 · 2023: 11 · 2022: 14 · 2021: 11 · 2020: 14 · 2019: 15 · 2018: 12 · 2017: 9 · 2016: 9
FWCI: 1.50
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Genetics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of General Medical Sciences (R00GM090042, K99GM115822, F32GM108288)
Topics: Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords: nutritional immunity, host-pathogen interaction, iron acquisition, arms race, host range, virulence, microbial competition, evolutionary genetics, natural selection, infectious diseases
MeSH terms: Animals, Bacteria, Communicable Diseases, Biological Evolution, Fungi, Humans, Immunity, Innate, Iron, Selection, Genetic, Transferrin, Gene Expression, Ion Transport, Siderophores, Virulence Factors, Host-Pathogen Interactions

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Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy

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