Nutritional immunity: transition metals at the pathogen–host interface

Hood, M. Indriati; Skaar, Eric P.

doi:10.1038/nrmicro2836

Cited by 1,310 publications

(1,277 citation statements)

References 149 publications

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“…Of particular interest was our finding of the robust interaction between carriage with manganese and copper. Copper is a required nutrient for C. albicans (serving as a cofactor for C. albicans SODs which protect cells from oxidative stress [26]) and also has inherent antifungal and antimicrobial activity by participating in Fenton reactions to generate harmful reactive oxygen species [38,39]. Moreover, Histatin 5 binds copper with high affinity, and this increases the killing activity of the peptide [40].…”

Section: Discussionmentioning

confidence: 99%

Salivary metals, age, and gender correlate with cultivable oral Candida carriage levels

Norris

Friedman

Chen

et al. 2018

Journal of Oral Microbiology

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Background: Little is known about the normal range of metal levels in unstimulated saliva, nor whether these might impact Candida carriage in healthy individuals. Both are important in determining which populations are at risk for candidiasis, as the availability of metal ions can influence the growth and pathogenesis of Candida albicans. Objective: We quantified salivary metals of healthy individuals to determine the correlation with C. albicans oral colonization. Design: Unstimulated whole saliva was collected from healthy adults and plated to determine fungal carriage, and metal content was measured using ICP-mass spectrometry (ICP-MS). Results: Zinc was most abundant, followed by iron, copper, manganese, and nickel. Cultivable oral Candida carriage was found in 48% of people. Total protein levels did not differ in salivas from donors with or without carriage. However, innate fungicidal activity was increased in donors with carriage; correlations between levels of several metals were stronger in salivas with fungal carriage, indicating a shift in the oral environment. Concentrations of copper and manganese, as well as age and gender, were significantly predictive of carriage levels in a multiple regression model. Conclusions: Salivary copper and manganese content along with age and gender could be used as a predictive metric for individuals that are more susceptible to Candida overgrowth.

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Section: Discussionmentioning

confidence: 99%

Salivary metals, age, and gender correlate with cultivable oral Candida carriage levels

Norris

Friedman

Chen

et al. 2018

Journal of Oral Microbiology

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“…Pathogens that lack copper efflux systems colonize poorly in the mammalian lung, possibly because of an inability to detoxify increased levels of copper in the host tissue (21). Detoxification of intracellular copper is achieved by efflux via P-type ATPase and RND (resistancenodulation-cell division) family efflux systems (22). We observed that V. fischeri lacking the P-type ATPase CopA or components of the RND efflux system CusCFBA exhibited significant colonization defects in the INSeq analysis and in 1:1 colonizations.…”

Section: Discussionmentioning

confidence: 99%

Global discovery of colonization determinants in the squid symbiontVibrio fischeri

Brooks

Gyllborg

Cronin

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

105

120

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Animal epithelial tissue becomes reproducibly colonized by specific environmental bacteria. The bacteria (microbiota) perform critical functions for the host's tissue development, immune system development, and nutrition; yet the processes by which bacterial diversity in the environment is selected to assemble the correct communities in the host are unclear. To understand the molecular determinants of microbiota selection, we examined colonization of a simplified model in which the light organ of Euprymna scolopes squid is colonized exclusively by Vibrio fischeri bacteria. We applied highthroughput insertion sequencing to identify which bacterial genes are required during host colonization. A library of over 41,000 unique transposon insertions was analyzed before and after colonization of 1,500 squid hatchlings. Mutants that were reproducibly depleted following squid colonization represented 380 genes, including 37 that encode known colonization factors. Validation of select mutants in defined competitions against the wild-type strain identified nine mutants that exhibited a reproducible colonization defect. Some of the colonization factors identified included genes predicted to influence copper regulation and secretion. Other mutants exhibited defects in biofilm development, which is required for aggregation in host mucus and initiation of colonization. Biofilm formation in culture and in vivo was abolished in a strain lacking the cytoplasmic chaperone DnaJ, suggesting an important role for protein quality control during the elaboration of bacterial biofilm in the context of an intact host immune system. Overall these data suggest that cellular stress responses and biofilm regulation are critical processes underlying the reproducible colonization of animal hosts by specific microbial symbionts.H umans and other animals are often sterile before birth, from which point they immediately proceed to acquire environmental bacteria (1). The bacteria that reproducibly colonize animal hosts are critical for host tissue development, immune system development, and nutrient acquisition. The selection process by which the functional symbionts take residence in the animal from among the great diversity of environmental microbes is poorly understood, so model systems have been especially valuable to examine how specific patterns of colonization are shaped by the genetic makeup of the bacteria and the host environment (2).The light organ of the Hawaiian bobtail squid, Euprymna scolopes, is colonized exclusively by the Gram-negative luminous bacterium Vibrio fischeri. The host inhabits seawater containing 10 6 bacteria per milliliter, with V. fischeri comprising at most 0.02% of the environmental population (3). E. scolopes hatch without symbionts, but then rapidly acquire environmental bacteria and proceed to select for V. fischeri in a "winnowing" process that ensures colonization by only the specific symbiont (4). The squid-Vibrio system thus presents an opportunity to investigate the processes that underlie acquisition of s...

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“…The extent to which some of these proteins might be involved in copper detoxification has not been analyzed isolates of S. aureus (Loeffler et al 2013). Moreover, given the role of transition metals in the mammalian immune response, the presence of cadCA and copB/mco provides corresponding strains with an advantage (Hood and Skaar 2012). Interestingly, the epidemic ST22-IV has been replacing other MRSA clones from hospitals possibly due to enhanced virulence.…”

Section: Copper and Zinc Resistance In Gram-positive Bacteriamentioning

confidence: 99%

Survival in amoeba—a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a “copper pathogenicity island”

Hao

Lüthje

Qin

et al. 2015

Appl Microbiol Biotechnol

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The presence of metal resistance determinants in bacteria usually is attributed to geological or anthropogenic metal contamination in different environments or associated with the use of antimicrobial metals in human healthcare or in agriculture. While this is certainly true, we hypothesize that protozoan predation and macrophage killing are also responsible for selection of copper/zinc resistance genes in bacteria. In this review, we outline evidence supporting this hypothesis, as well as highlight the correlation between metal resistance and pathogenicity in bacteria. In addition, we introduce and characterize the Bcopper pathogenicity island^identified in Escherichia coli and Salmonella strains isolated from copper-and zinc-fed Danish pigs.

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Nutritional immunity: transition metals at the pathogen–host interface

Cited by 1,310 publications

References 149 publications

Salivary metals, age, and gender correlate with cultivable oral Candida carriage levels

Salivary metals, age, and gender correlate with cultivable oral Candida carriage levels

Global discovery of colonization determinants in the squid symbiontVibrio fischeri

Survival in amoeba—a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a “copper pathogenicity island”

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