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Availability of Ferritin-Bound Iron to Enterobacteriaceae

Gehrer, Clemens M., Hoffmann, Alexander, Hilbe, Richard, Grubwieser, Philipp, Mitterstiller, Anna-Maria, Talasz, Heribert, Fang, Ferric C., Meyron-Holtz, Esther G., Atkinson, Sarah H., Weiss, Günter, Nairz, Manfred·2022·International Journal of Molecular Sciences
DOI 10.3390/ijms232113087PMC PMC9657528
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Abstract

The sequestration of iron in case of infection, termed nutritional immunity, is an established strategy of host defense. However, the interaction between pathogens and the mammalian iron storage protein ferritin is hitherto not completely understood. To better characterize the function of ferritin in Gram-negative infections, we incubated iron-starved cultures of Salmonella Typhimurium and knockout mutant strains defective for major iron uptake pathways or Escherichia coli with horse spleen ferritin or ionic iron as the sole iron source. Additionally, we added bovine superoxide dismutase and protease inhibitors to the growth medium to assess the effect of superoxide and bacterial proteases, respectively, on Salmonella proliferation and reductive iron release. Compared to free ionic iron, ferritin-bound iron was less available to Salmonella, but was still sufficient to significantly enhance the growth of the bacteria. In the absence of various iron acquisition genes, the availability of ferritin iron further decreased. Supplementation with superoxide dismutase significantly reduced the growth of the ΔentC knockout strain with holoferritin as the sole iron source in comparison with ionic ferrous iron. In contrast, this difference was not observed in the wildtype strain, suggesting that superoxide dismutase undermines bacterial iron uptake from ferritin by siderophore-independent mechanisms. Ferritin seems to diminish iron availability for bacteria in comparison to ionic iron, and its iron sequestering effect could possibly be enhanced by host superoxide dismutase activity.

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Figure 1 Growth of (a) S.Tm (N = 15, n = 5) and (b) E. coli (N = 15, n = 8) upon supplementation of ferrous iron and holoferritin at rising iron concentrations. Utilization of apoferritin by (c) S.Tm and (d) E. coli in equal protein concentrations corresponding to holoferritin containing 5 and 50 µM of iron (0.0028 and 0.0282 µM apoferritin, respectively; N = 15, n = 5). The addition of apoferritin resulted in a very small increase in the iron content of the final solution, which we calculated to be 1.121 and 11.221 nM for the low and high apoferritin group, respectively. Growth of (e) S.Tm (N = 15, n = 5) and (f) E. coli (N = 15, n = 5) upon the addition of 50 µM iron as ferrous iron or holoferritin normalized to their respective control: For ferrous iron, IMDM alone, whereas for holoferritin, apoferritin in equimolar protein concentration was used for normalization. (g) The growth-promoting effect of apoferritin on S.Tm upon addition of a PIC. All cultures were grown aerobically in ambient air at 37 °C and were shaken at 200 RPM. Growth data were logarithmized and then normalized to their corresponding control. Graphs are depicted as mean ± SD. (a,b) Two-way ANOVA or (c,d) one-way ANOVA corrected for multiple comparisons with the Holm-Sidak post hoc test was used. (e–g) Student’s t-test was used (*: p < 0.05; **: p < 0.01; ***: p < 0.001, ****: p < 0.0001). N: number of biological replicates, n: number of experiments conducted, PIC: protease inhibitor cocktail.
Figure 1 Growth of (a) S.Tm (N = 15, n = 5) and (b) E. coli (N = 15, n = 8) upon supplementation of ferrous iron and holoferritin at rising iron concentrations. Utilization of apoferritin by (c) S.Tm and (d) E. coli in equal protein concentrations corresponding to holoferritin containing 5 and 50 µM of iron (0.0028 and 0.0282 µM apoferritin, respectively; N = 15, n = 5). The addition of apoferritin resulted in a very small increase in the iron content of the final solution, which we calculated to be 1.121 and 11.221 nM for the low and high apoferritin group, respectively. Growth of (e) S.Tm (N = 15, n = 5) and (f) E. coli (N = 15, n = 5) upon the addition of 50 µM iron as ferrous iron or holoferritin normalized to their respective control: For ferrous iron, IMDM alone, whereas for holoferritin, apoferritin in equimolar protein concentration was used for normalization. (g) The growth-promoting effect of apoferritin on S.Tm upon addition of a PIC. All cultures were grown aerobically in ambient air at 37 °C and were shaken at 200 RPM. Growth data were logarithmized and then normalized to their corresponding control. Graphs are depicted as mean ± SD. (a,b) Two-way ANOVA or (c,d) one-way ANOVA corrected for multiple comparisons with the Holm-Sidak post hoc test was used. (e–g) Student’s t-test was used (*: p < 0.05; **: p < 0.01; ***: p < 0.001, ****: p < 0.0001). N: number of biological replicates, n: number of experiments conducted, PIC: protease inhibitor cocktail.CC BY · PubMed Central
Figure 2 S.Tm ATCC 14028 and derivative knockout mutant strains were grown (a) without any supplement (N = 15, n = 5) or (b) with the addition of 4mM of n-acetylcysteine (N = 15, n = 5). Growth of the same strains with 5 µM (c) of ferrous iron (N = 15, n = 5), (d) of ferric iron (N = 12, n = 5) or (e) of ferritin-bound iron as sole iron source (N = 15, n = 5). Growth data were logarithmized and then normalized to the WT without any iron supplement. Graphs are depicted as mean ± SD. For statistical analysis (a–e) one-way ANOVA corrected for multiple comparisons with the Holm-Sidak post hoc test was used (***: p < 0.001, ****: p < 0.0001, numbers indicate a non-significant p-value > 0.05). N: number of biological replicates, n: number of experiments conducted, WT: wildtype, ΔentC: S.Tm enterobactin/salmochelin knockout mutant strain, Δtriple: combined knockout mutant strain of entC, sit and feo.
Figure 2 S.Tm ATCC 14028 and derivative knockout mutant strains were grown (a) without any supplement (N = 15, n = 5) or (b) with the addition of 4mM of n-acetylcysteine (N = 15, n = 5). Growth of the same strains with 5 µM (c) of ferrous iron (N = 15, n = 5), (d) of ferric iron (N = 12, n = 5) or (e) of ferritin-bound iron as sole iron source (N = 15, n = 5). Growth data were logarithmized and then normalized to the WT without any iron supplement. Graphs are depicted as mean ± SD. For statistical analysis (a–e) one-way ANOVA corrected for multiple comparisons with the Holm-Sidak post hoc test was used (***: p < 0.001, ****: p < 0.0001, numbers indicate a non-significant p-value > 0.05). N: number of biological replicates, n: number of experiments conducted, WT: wildtype, ΔentC: S.Tm enterobactin/salmochelin knockout mutant strain, Δtriple: combined knockout mutant strain of entC, sit and feo.CC BY · PubMed Central
Figure 3 (a) Growth of S.Tm upon addition of a PIC (N = 3, n = 2). (b) Effect of the individual protease inhibitors of the PIC (excluding Bestatin hydrochloride, which was not available due to shortness of supplies, AEBSF: 346.67 µM, E64: 4.67 µM, Aprotinin: 0.27 µM, Leupeptin: 6.67 µM, Pepstatin A: 5 µM), on the growth of S.Tm with 5 µM of ferritin-bound iron (N = 3, n = 1). Growth of (c) WT S.Tm (N = 15, n = 5) and (d) the ΔentC strain upon addition of AEBSF to the medium (N = 12, n = 4). Growth of (e) the WT strain (N = 15, n = 4) and (f) the ΔentC mutant (N = 12, n = 4) upon addition of ferrous or ferritin bound iron with or without AEBSF (triangles and circles, respectively). (a,b) were conducted in ambient air and (c–f) were conducted in 5% O2, 5% CO2 atmosphere. Growth data were logarithmized and then normalized to (a,c,d) the iron free control, (b) supplementation with 5 µM of ferritin-bound iron, or (e,f) their corresponding controls: no supplement (circles) or AEBSF (triangles), to account for the iron-independent growth inhibition of AEBSF. Graphs are depicted as mean ± SD. For statistical analysis, either Student’s t-test (c,d) or one-way ANOVA (e,f) corrected for multiple comparisons, and the Holm-Sidak post hoc test was also used (*: p < 0.05; ****: p < 0.0001, numbers indicate a non-significant p-value > 0.05). N: number of biological replicates, n: number of experiments conducted, PIC: protease inhibitor cocktail, WT: wildtype S.Tm, ΔentC: S.Tm enterobactin/salmochelin knockout mutant strain, AEBSF: 4-(2-Aminoethyl)benzenesulfonyl fluoride.
Figure 3 (a) Growth of S.Tm upon addition of a PIC (N = 3, n = 2). (b) Effect of the individual protease inhibitors of the PIC (excluding Bestatin hydrochloride, which was not available due to shortness of supplies, AEBSF: 346.67 µM, E64: 4.67 µM, Aprotinin: 0.27 µM, Leupeptin: 6.67 µM, Pepstatin A: 5 µM), on the growth of S.Tm with 5 µM of ferritin-bound iron (N = 3, n = 1). Growth of (c) WT S.Tm (N = 15, n = 5) and (d) the ΔentC strain upon addition of AEBSF to the medium (N = 12, n = 4). Growth of (e) the WT strain (N = 15, n = 4) and (f) the ΔentC mutant (N = 12, n = 4) upon addition of ferrous or ferritin bound iron with or without AEBSF (triangles and circles, respectively). (a,b) were conducted in ambient air and (c–f) were conducted in 5% O2, 5% CO2 atmosphere. Growth data were logarithmized and then normalized to (a,c,d) the iron free control, (b) supplementation with 5 µM of ferritin-bound iron, or (e,f) their corresponding controls: no supplement (circles) or AEBSF (triangles), to account for the iron-independent growth inhibition of AEBSF. Graphs are depicted as mean ± SD. For statistical analysis, either Student’s t-test (c,d) or one-way ANOVA (e,f) corrected for multiple comparisons, and the Holm-Sidak post hoc test was also used (*: p < 0.05; ****: p < 0.0001, numbers indicate a non-significant p-value > 0.05). N: number of biological replicates, n: number of experiments conducted, PIC: protease inhibitor cocktail, WT: wildtype S.Tm, ΔentC: S.Tm enterobactin/salmochelin knockout mutant strain, AEBSF: 4-(2-Aminoethyl)benzenesulfonyl fluoride.CC BY · PubMed Central
Figure 4 Iron-dependent growth of (a) WT S.Tm (N = 15, n = 5) and (b) the ΔentC strain with or without SOD, depicted as squares and circles, respectively (N = 12, n = 4). Fold change in RyhB1 sncRNA expression normalized to the mean of the corresponding iron-free control of (c) WT S.Tm (N = 9, n = 3) and (d) the ΔentC strain upon different iron sources with and without SOD (N = 12, n = 4). Fold change in ahpC expression normalized to the mean of the corresponding iron-free control of (e) WT S.Tm (N = 9, n = 3) and (f) the ΔentC strain upon different iron sources with and without SOD (N = 12, n = 4). (c,e) In the WT a higher concentration of SOD was used in order to ensure complete dismutation of O2- to assess a possible involvement of the catalytic mechanism with strong iron(III) ligands [57]. Cultures were incubated at 5% O2 5% CO2, 37 °C and 200 RPM. Growth data were logarithmized and then normalized to the corresponding control without any supplement. Expression data were normalized to their corresponding controls: no supplement (circles) or SOD (squares). Gene expression was normalized using the ΔΔct method using the 16S ribosomal RNA (16S rRNA) and DNA-dependent RNA polymerase (rpoB) mRNA as reference transcripts. Graphs are depicted as mean ± SD. For statistical analysis, one-way ANOVA (a–f) corrected for multiple comparisons when the Holm-Sidak post hoc test was used (*: p < 0.05, ****: p < 0.0001, numbers indicate a non-significant p-value > 0.05). N: number of biological replicates, n: number of experiments conducted. SOD: superoxide dismutase, WT: wildtype S.Tm, ΔentC: S.Tm enterobactin/salmochelin knockout mutant strain, SOD: superoxide dismutase.
Figure 4 Iron-dependent growth of (a) WT S.Tm (N = 15, n = 5) and (b) the ΔentC strain with or without SOD, depicted as squares and circles, respectively (N = 12, n = 4). Fold change in RyhB1 sncRNA expression normalized to the mean of the corresponding iron-free control of (c) WT S.Tm (N = 9, n = 3) and (d) the ΔentC strain upon different iron sources with and without SOD (N = 12, n = 4). Fold change in ahpC expression normalized to the mean of the corresponding iron-free control of (e) WT S.Tm (N = 9, n = 3) and (f) the ΔentC strain upon different iron sources with and without SOD (N = 12, n = 4). (c,e) In the WT a higher concentration of SOD was used in order to ensure complete dismutation of O2- to assess a possible involvement of the catalytic mechanism with strong iron(III) ligands [57]. Cultures were incubated at 5% O2 5% CO2, 37 °C and 200 RPM. Growth data were logarithmized and then normalized to the corresponding control without any supplement. Expression data were normalized to their corresponding controls: no supplement (circles) or SOD (squares). Gene expression was normalized using the ΔΔct method using the 16S ribosomal RNA (16S rRNA) and DNA-dependent RNA polymerase (rpoB) mRNA as reference transcripts. Graphs are depicted as mean ± SD. For statistical analysis, one-way ANOVA (a–f) corrected for multiple comparisons when the Holm-Sidak post hoc test was used (*: p < 0.05, ****: p < 0.0001, numbers indicate a non-significant p-value > 0.05). N: number of biological replicates, n: number of experiments conducted. SOD: superoxide dismutase, WT: wildtype S.Tm, ΔentC: S.Tm enterobactin/salmochelin knockout mutant strain, SOD: superoxide dismutase.CC BY · PubMed Central

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Metadata

Authors
Gehrer, C. M., Hoffmann, A., Hilbe, R., Grubwieser, P., Mitterstiller, A.-M., Talasz, H., Fang, F. C., Meyron-Holtz, E. G., Atkinson, S. H., Weiss, G., & Nairz, M.
Affiliations
  • Department of Internal Medicine II, Infectious Diseases, Immunology, Rheumatology, Medical University of Innsbruck, 6020 Innsbruck, Austria
  • Biocenter, Institute of Medical Biochemistry, Medical Universitiy of Innsbruck, 6020 Innsbruck, Austria
  • Department of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, WA 98195-7110, USA
  • Laboratory of Molecular Nutrition, Faculty of Biotechnology and Food Engineering, Technion-Israel Institute of Technology, Haifa 32000, Israel
  • Kenya Medical Research Institute (KEMRI), Centre for Geographic Medicine Research Coast, KEMRI-Wellcome Trust Research Programme, Kilifi 80108, Kenya
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2022-10-28
Volume
23
Issue
21
Pages
13087
ISSN
1422-0067
DOI
10.3390/ijms232113087
PMC
PMC9657528
Cited by
10
References
15
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Austrian Science Fund (FWF) (P 33062-B)

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