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Nanozymes modulate probiotic tryptophan metabolism to prevent Salmonella infection in mammalian models

Nature Microbiology volume 10, pages 3272–3289 (2025)Cite this article

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Abstract

Probiotics are promising alternatives to antibiotics for the treatment of intestinal infections, but the effects of probiotics alone are often insufficient. Here we uncovered synergism between antibacterial iron–sulfur nanozymes (nFeS) and tryptophan derivatives that protects mice and pigs against bacterial gut infections. nFeS selectively inhibited potential intestinal pathogens while sparing commensal Lactobacillus vaginalis, whose presence enhanced the protective activity of nFeS against Salmonella enterica subsp. enterica serovar Typhimurium in vivo. Metabolomics and mutational analysis revealed that L. vaginalis synthesized 2-indolecarboxylic acid from a tryptophan derivative, indole-3-carboxaldehyde, a reaction that was catalysed by nFeS. The cytoplasmic pH of L. vaginalis (pH 7.5) allowed 2-indolecarboxylic acid to chelate free ferrous ions released by nFeS, thereby protecting it from antibacterial effects, whereas pathogens such as S. Typhimurium with a lower cytoplasmic pH were susceptible (pH 6.5). Pretreatment of pigs and mice with L. vaginalis and nFeS protected them against Salmonella infection. Our findings provide a foundation for improving probiotic bacteria-based therapies against intestinal infections.

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Fig. 1: nFeS improves gut homeostasis through preferentially suppressing intestinal pathogenic bacteria.
Fig. 2: Gut microbiota and L. vaginalis facilitate nFeS action in resisting S. Typhimurium infection.
Fig. 3: nFeS expands the microbial tryptophan–indole pathway to produce I2CA.
Fig. 4: nFeS catalyses the conversion of I3C to I2CA via isomerase-like and oxygenase-like activities.
Fig. 5: I2CA is critical for the tolerance of L. vaginalis to nFeS and selective antibacterial action.
Fig. 6: nFeS combined with L. vaginalis prevents S. Typhimurium infection.

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Data availability

All data needed to evaluate the conclusions are presented in the article and its Extended Data Figs. 1–10 and Supplementary Information. Raw data can be found in the source data files for each figure item. Source data are provided with this paper and are available via figshare at https://doi.org/10.6084/m9.figshare.29652707 (ref. 110). The 16S rRNA gene sequencing data of gut microbiota have been deposited in the NCBI Sequence Read Archive under PRJNA1314424 and PRJNA1314429. Metabolomic (weaned piglets, mice and L. vaginalis) sequencing data have been deposited in CNGBdb under CNP0006014, CNP0006015 and CNP0006017. Transcriptomic sequencing of L. vaginalis has been deposited in NCBI Sequence Read Archive under PRJNA1310755.

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Acknowledgements

We thank Z. Wang (Institute of Atomic and Molecular Physics, Jilin University) for their technical support in the DFT simulations. We thank P. He (State Key Laboratory of Animal Nutrition and Feeding, Department of Animal Nutrition and Feed Science, China Agricultural University) and A. Liu (State Key Laboratory of Animal Nutrition and Feeding, Department of Animal Nutrition and Feed Science, China Agricultural University) for liquid chromatography–mass spectrometry. We thank P. Liu (College of Animal Sciences, Fujian Agriculture and Forestry University) for the piglet sample collection. This work is supported by the National Key Research and Development Program of China (grant no. 2023YFD1301103 for B.D.), the Special Fund for Strategic Pilot Technology of Chinese Academy of Sciences (grant no. XDC0120200 for L.G.) and the National Natural Science Foundation of China (grant nos. 22121003 for L.G. and 32260859 for B.D.).

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Authors and Affiliations

  1. State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University, Beijing, China

    Zishen Lin, Jinping Wang, Lixue Wang, Ying Zhang & Bing Dong

  2. College of Animal Sciences, Fujian Agriculture and Forestry University, Fuzhou, China

    Yue Feng

  3. CAS Engineering Laboratory for Nanozyme, State Key Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

    Lei Chen, Qian Wang, Haolin Cao, Jing Jiang & Lizeng Gao

  4. Institute of Fundamental and Frontier Sciences, University of Electronic Science and Technology of China, Chengdu, China

    Yang Gao

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Contributions

B.D., L.G. and Z.L. conceived of this study. Z.L. performed the bioinformatics and statistical analyses on the sequencing data, and performed and analysed the results of redox potential assays, Raman spectrometry and FTIR. Z.L. and Y.F. designed the biological experiments and carried out the experiments with J.W., Q.W., L.W. and Y.Z. L.C., H.C., J.J. and Y.G. conducted the DFT calculations. Z.L., B.D. and L.Z.G. wrote the paper with input from Y.F., L.C., H.C. and Y.G. All authors approved the final draft of the paper.

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Correspondence to Lizeng Gao or Bing Dong.

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Nature Microbiology thanks Nico Claassens, Till Strowig and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Microbiota sequence enriches microbial ferroptosis pathway induced by nFeS.

a Relative protein expression of claudin-1, glutathione peroxidase (GPX4), and NADPH oxidase 1 (NOX1) in the gut epithelium (n = 3 samples). b Sobs index of alpha diversity between CON and nFeS group in genus and family levels (n = 5 piglets). c Venn plot analysis. d Relative abundance of Lactobacteriaceae in family level (n = 5 piglets). e Relative abundance of Fusicatenibacter in genus level (n = 5 piglets). f Antibacterial effect of nFeS to L. vaginalis. g, h MDA level (n = 5 L. vaginalis) and ROS species generation (n = 3 L. vaginalis) change in nFeS-treated L. vaginalis. i Growth curve of L. vaginalis. j Comparison of absorbance (OD600) of L. vaginalis treated with nFeS or Na2S3 (n = 3 L. vaginalis). k Correlation between bacteria killed by nFeS (related to Fig. 1l, m) with levels of serum DAO and IL-1β. l Faecal SCFA levels (n = 5 piglets). m Correlation between bacteria killed by nFeS (related to Fig. 1l, m) and faecal SCFA levels. n Spearman analysis between differential bacteria abundance and relative gene levels, serum DAO and IL-1β levels, and the functions of the bacterial communities (ferroptosis, pentose phosphate pathway, cytochrome c oxidase, and glutamate synthase). These functions of the bacterial communities were predicted with PICRUSt2 of 16S rRNA sequencing using the Kyoto Encyclopaedia of Genes and Genomes (KEGG) database and had significant difference between the CON and nFeS groups. P values were calculated using a two-sided unpaired t-test. Spearman analysis of k, m, n are at the two-sided 99% confidence interval, and the significance marked in the figures. Data were shown as the standard error of the mean. Exact P values of a-d, d-e, g, j, and l are displayed in the figure. Each experiment was repeated independently for three times with similar results.

Source data

Extended Data Fig. 2 Antibacterial action of nFeS towards S. aureus, S. Typhimurium, and E. coli correlates to ferrous iron.

a Antibacterial ability of nFeS was shown as antibacterial diameter in the agar plate included S. aureus, S. Typhimurium, and E. coli. DOX was doxycycline. The diameter of the inhibition zone is measured in millimetres. b Antibacterial ability of nFeS to suppress the growth of S. aureus, S. Typhimurium, and E. coli in liquid culture media (n = 3 bacteria per treatment). c Concentration of ferrous iron ion accumulated in the supernatant of S. aureus, S. Typhimurium, E. coli in the different doses of nFeS (n = 3 bacteria per treatment). d, e Antibacterial ability of FeCl2 and Na2S3 to suppress the growth of S. aureus, S. Typhimurium, and E. coli in liquid culture media, respectively (n = 3 bacteria per treatment). f Generation of ROS in S. Typhimurium with nFeS treatment (n = 3 bacteria per treatment). g Changes of MDA level in S. aureus, S. Typhimurium, and E. coli with nFeS treatment (n = 5 bacteria per treatment). P values were calculated using a two-sided unpaired t-test. Data were shown as the standard error of the mean. Exact P values are displayed in the figure. Each experiment was repeated independently for three times with similar results.

Source Data

Extended Data Fig. 3 nFeS along with L. vaginalis improves gut epithelial heath, without inducing host ferroptosis.

a Faecal iron element was detected every day from the first gavage day to the 7th day of the end of gavage. Mice that received 5 mg/kg body weight (BW) nFeS for 7 days adapted a concentration balance of nFeS in the intestine, and excreted out by a-five-day after stopping gavage (n = 3 mice). b Changes of MDA level in gut epithelium of mice (n = 6 mice). c Relative mRNA levels of GPX4, FTH-1, NCOA4, ACSL4, NOX1, and COX2 in gut epithelium of mice (n = 6 mice). d Changes of colonic length (n = 6 mice). e Serum IL-1β and IL-6 levels (n = 6 mice). f Faecal SCFA levels (n = 6 mice). g Relative protein levels of FTH-1 and GPX4 in the gut epithelium of mice (n = 3 samples). h Relative mRNA levels of COX2, ACSL4, and NCOA4 in gut epithelium of mice (n = 6 mice). i Changes of MDA level in gut epithelium of mice (n = 6 mice). j ROS generation in the gut epithelial cells of mice (n = 3 mice). P values were calculated using ordinary one-way ANOVA followed by Tukey’s test (b-d, g) or Benjamini, Krieger & Yekutieli (e, f) for multiple comparisons. Data were shown as the standard error of the mean. Exact P values are displayed in the figure (P < 0.0001; the exact P value is < 0.0001). Each experiment was repeated independently for three times with similar results.

Source Data

Extended Data Fig. 4 Antibacterial tryptophan-indole metabolites of L. vaginalis are beyond 3-HAA, ILA, I3CA, and metabolites of serotonin pathway.

a, b Antibacterial abilities of L. vaginalis (included supernatant and sediment) towards S. aureus, S. Typhimurium, and E. coli tested in agar plate (n = 3 L. vaginalis). c PCoA of Bray-Curtis dissimilarity matrices and Venn plot were generated from the non-targeted metabolomics data of L. vaginalis, weaned piglets, and mice. d Kynurenine and serotonin pathways are showed as microbial pathways in tryptophan pathway27. 3-HAA is the end product of the kynurenine/IDO signalling pathway, and 5HIAA and melatonin are the end products of the serotonin pathway. e Relative abundance of 3-HAA, 5-HTP, 5-HT, 5-HIAA, and melatonin in L. vaginalis, weaned piglets, and mice. 3-HAA and 5-HT were not captured in L. vaginalis metabolites. 5-HTP was not captured in metabolites of weaned piglets. 5-HIAA and melatonin were not detected in metabolites of weaned piglets and L. vaginalis (n = 4 (CON/SM + LV) or 5 (SM/SM + LV+nFeS) mice per group, 5 piglets per group, and 6 L. vaginalis per group). f Common pathway, I3C/I3CA/I2CA, in L. vaginalis, weaned piglets, and mice. g Antibacterial ability of ILA to inhibit growth of S. aureus, S. Typhimurium, and E. coli. h Antibacterial abilities of I3CA alone and I3CA co-treated with nFeS to inhibit growth of S. aureus, S. Typhimurium, and E. coli (n = 3 samples). P values were calculated using a two-sided unpaired t-test for two-group comparisons and ordinary one-way ANOVA followed Benjamini, Krieger & Yekutieli for multiple comparisons. Data were shown as the standard error of the mean. The diameter of the inhibition zone is measured in millimetres (mm). Exact P values are displayed in the figure (P < 0.0001; the exact P value is < 0.0001). Each experiment was repeated independently for three times with similar results. Panel f was created with BioRender.com.

Source Data

Extended Data Fig. 5 nFeS enhances the transcription level of sugar transporters and the metabolic level of TCA cycle to promote L. vaginalis viability.

a PCoA analysis of transcriptome in the L. vaginalis on Bray-Curtis dissimilarity matrices. b Venn plot of transcriptome in the L. vaginalis between the CON and nFeS group. c Changes of differential up-regulated genes in L. vaginalis with nFeS treatment among the first 20 altered genes. d KEGG enrichment of transcriptome in L. vaginalis with nFeS treatment. e Changes of monosaccharide compounds in the metabolic pathway of L. vaginalis (n = 6 L. vaginalis). f Relative abundance of significantly changed intermediate metabolites of TCA cycle in L. vaginalis (n = 6 L. vaginalis). g Changes of saccharide compounds in the metabolic pathway of weaned piglets (n = 5 piglets). h Relative abundance of significant change intermediate metabolites of TCA cycle in weaned piglets (n = 5 piglets). i Changes of monosaccharide compounds in the metabolic pathway of mice (n = 4 (CON/SM + LV) or 5 (SM/SM + LV+nFeS) mice per group). j Relative abundance of significant change intermediate metabolites of TCA cycle in mice (n = 4 (CON/SM + LV) or 5 (SM/SM + LV+nFeS) mice per group). P values were calculated using a two-sided unpaired t-test for two-group comparisons and ordinary one-way ANOVA followed Benjamini, Krieger & Yekutieli for multiple comparisons. Data were shown as the standard error of the mean. Exact P values are displayed in the figure (P < 0.0001; the exact P value is < 0.0001). Each experiment was repeated independently for three times with similar results. Panels e, g and i were created with BioRender.com.

Source Data

Extended Data Fig. 6 Alcohol dehydrogenase is the upstream enzyme to produce I3C as the substrate for nFeS catalysis in L. vaginalis.

a Amino acid sequences of methanol dehydrogenase in Lactobacillus spp. were compared with 7 kinds of alcohol dehydrogenases (adH1-7) in L. vaginalis by TM-align comparisons. The adH3 gene was identified to potentially be the gene encoding methanol dehydrogenase in L. vaginalis. b Establishment of pUC19-pLV-adH-OE and pUC19-adH-Mut recombinant plasmids to overexpress or knock out adH3 (L. vaginalisOE or L. vaginalisMut). c Relative mRNA level of adH (n = 3 L. vaginalisWT/OE/Mut). d Detection of I3C, I3CA, and I2CA concentration in L. vaginalisOE and L. vaginalisMut (supernatant and sediment) (n = 3 L. vaginalisWT/OE/Mut). e Detection of I3C, I3CA, and I2CA concentration in L. vaginalisWT, L. vaginalisOE, and L. vaginalisMut (bacteria sediment) receiving nFeS treatment (n = 3 L. vaginalisWT/OE/Mut). f Characterization of nFeS in L. vaginalis by transmission electron microscopy (Scale bar at 100 nm). P values were calculated using a two-sided unpaired t-test for two-group comparisons. Data were shown as the standard error of the mean. Exact P values are displayed in the figure. Each experiment was repeated independently for three times with similar results. Panel b was created with BioRender.com.

Source Data

Extended Data Fig. 7 Recyclability of nFeS in the conversion from I3C to I2CA confirms its catalytic behavior.

a nFeS and Fe3O4 were reacted with I3C and I3CA, respectively, then recycled nFeS and Fe3O4 to next reaction with new weigh I3C and I3CA. b-e I3C, I3CA, and I2CA concentration at the end of five times of recycled reaction. nFeS is represented as Fe3S4 here. f Different concentrations of I3C as substrates reacted with nFeS (After 5 times recycled), the generation rate of I2CA per unit time was used to fit the Michaelis–Menten curve of enzyme kinetic reaction. g Concentration changes of I2CA in the reaction between I3C and nFeS during 240 min. h Redox potential of nFeSOx/nFeSRe and I3CA/I3C couples. i Standard redox potentials of NAD+/NADH, nFeSOx2/nFeSRe2, O2/HO2−, I3CA/I3C, O2/OH−, nFeSOx1/nFeSRe1, O2/H2O2, and O2/H2O. Ox represents the oxidation state. Re indicates the reduced state. Each experiment was repeated independently for three times with similar results. Panel a was created with BioRender.com.

Source Data

Extended Data Fig. 8 I2CA enables ferrous iron outside of L. vaginalis and synergizes with nFeS against pathogenic bacteria.

a Concentration of ferrous ions accumulated in the supernatant of L. vaginalis (removed the nFeS) in the different doses of nFeS. b Concentration of ferrous ions accumulated in the supernatant of L. vaginalisWT, L. vaginalisOE, L. vaginalisMut. c Changes of intracellular pH of bacteria in different extracellular pH conditions. d Intracellular pH values of different bacteria under nFeS treatment. e Changes of intracellular pH of bacteria, which were allowed to grow to a relative density (OD600 = 0.8) followed by nFeS treatment (1 mg/ml) and/or I2CA (1 mg/ml) for 12 hours. f Characterization of bactericidal abilities of I2CA, I3CA, combined utilization of I2CA and nFeS to S. aureus, S. Typhimurium, E. coli (after treating 8 hours), scale bar at 1 µm. g Level of AKP in the supernatant of S. aureus, S. Typhimurium, E. coli (after treating 24 hours) (n = 6 (CON/12CA/12CA+nFeS) or n = 4 (I3CA) samples per group). h Turbidity and growth of S. aureus, S. Typhimurium, E. coli in treatment of I2CA, I3CA, I2CA+nFeS for 24 hours, respectively. P values were calculated using ordinary one-way ANOVA followed Benjamini, Krieger & Yekutieli for multiple comparisons. Data were shown as the standard error of the mean. Exact P values are displayed in the figure (P < 0.0001; the exact P value is < 0.0001). Each experiment was repeated independently for three times with similar results.

Source Data

Extended Data Fig. 9 nFeS is biocompatible with multiple probiotics.

Relative abundance of significant changed probiotics in colonic chyme of weaned piglets (n = 5 piglets). P values were calculated using ordinary one-way ANOVA or Kruskal-Wallis test followed Benjamini, Krieger & Yekutieli for multiple comparisons. Data were shown as the standard error of the mean. Exact P values are displayed in the figure (P < 0.0001; the exact P value is < 0.0001).

Extended Data Fig. 10 Pathogenic and opportunistic pathogenic bacteria are sensitive to single or combined nFeS with L. vaginalis.

Relative abundance of significant changed pathogenic and opportunistic bacteria in colonic chyme of weaned piglets (n = 5 piglets). P values were calculated using ordinary one-way ANOVA followed Benjamini, Krieger & Yekutieli for multiple comparisons. Data were shown as the standard error of the mean. Exact P values are displayed in the figure (P < 0.0001; the exact P value is < 0.0001).

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Lin, Z., Feng, Y., Chen, L. et al. Nanozymes modulate probiotic tryptophan metabolism to prevent Salmonella infection in mammalian models. Nat Microbiol 10, 3272–3289 (2025). https://doi.org/10.1038/s41564-025-02176-4

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