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Systematic discovery of antibacterial and antifungal bacterial toxins

Nature Microbiology volume 9, pages 3041–3058 (2024)Cite this article

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An Author Correction to this article was published on 19 February 2025

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Abstract

Microorganisms use toxins to kill competing microorganisms or eukaryotic cells. Polymorphic toxins are proteins that encode carboxy-terminal toxin domains. Here we developed a computational approach to identify previously undiscovered, conserved toxin domains of polymorphic toxins within 105,438 microbial genomes. We validated nine short toxins, showing that they cause cell death upon heterologous expression in either Escherichia coli or Saccharomyces cerevisiae. Five cognate immunity genes that neutralize the toxins were also discovered. The toxins are encoded by 2.2% of sequenced bacteria. A subset of the toxins exhibited potent antifungal activity against various pathogenic fungi but not against two invertebrate model organisms or macrophages. Experimental validation suggested that these toxins probably target the cell membrane or DNA or inhibit cell division. Further characterization and structural analysis of two toxin–immunity protein complexes confirmed DNase activity. These findings expand our knowledge of microbial toxins involved in inter-microbial competition that may have the potential for clinical and biotechnological applications.

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Fig. 1: Computational prediction of toxin domains (PTs) and cognate immunity genes (PIM genes) in polymorphic toxin proteins.
Fig. 2: PTs efficiently kill bacteria and/or yeast and PIM genes neutralize the toxicity.
Fig. 3: Critical residues and predicted protein structures of the PTs.
Fig. 4: Antibacterial and antifungal activities of PT toxins.
Fig. 5: PT4Ec and PT9Ec of E. coli strain 48 exhibit broad-spectrum antifungal activity.
Fig. 6: Biochemical and structural characterization of PT1Em and PT7Bc mechanisms of action.

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Data availability

All of the raw data were deposited at https://doi.org/10.5281/zenodo.13341769 (ref. 59). Accession codes for the sequences can be found in Supplementary Table 2. The required information for the structural analysis is presented in Supplementary Table 10.

Code availability

The main scripts used in the analysis have been deposited at https://github.com/noamdotan/levylab.

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Acknowledgements

A.L. is generously supported by the Israel Science Foundation (grants 1535/20, 3300/20 and 3062/20), Israeli Ministry of Innovation, Science and Technology (grant 1001695377) and Israel Innovation Authority (grant 81259). N.N. is supported by the Israel Science Foundation (grant 1535/20) and a PhD scholarship from the Faculty of Agriculture, Food and Environment at the Hebrew University of Jerusalem. N.T. is supported by the Israel Science Foundation (grants 1600/21 and 1818/21). N.S. is supported by the Israel Science Foundation (grant 1760/20), Zuckerman STEM Leadership Program, Ministry of Science and Technology of Israel (grant 0001998) and BARD US–Israel Agricultural Research and Development Fund (grant IS-5492-22 R). M.K. and J.K. are supported by the European Research Council (Advanced Grant 743016). We thank R. Stephan at the University of Zurich, Switzerland for providing Shiga toxin-producing E. coli strain 48 and M. Morand at the Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences for help with the liposome-based assays. We thank members of A. Levy’s laboratory for critical reading, advice and helpful discussions throughout, especially A. Geller and A. Bograd. We thank M. Canjalli for helping with some of the experiments with fungi. We thank the ESRF for the provision of synchrotron radiation facilities and ESRF ID30A local contacts for support and help during data collection.

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Author notes

  1. These authors contributed equally: Nimrod Nachmias, Noam Dotan, Marina Campos Rocha.

Authors and Affiliations

  1. Department of Plant Pathology and Microbiology, Institute of Environmental Sciences, Robert H. Smith Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, Rehovot, Israel

    Nimrod Nachmias, Noam Dotan, Maor Shalom, Shani Cheskis, Gilad Meitav, Arbel Rivitz, Naama Shamash-Halevy, Yaara Oppenheimer-Shaanan & Asaf Levy

  2. Koret School of Veterinary Medicine, Robert H. Smith Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, Rehovot, Israel

    Marina Campos Rocha & Neta Shlezinger

  3. Department of Biological Chemistry, Alexander Silberman Institute of Life Sciences, Faculty of Mathematics and Science, Hebrew University of Jerusalem, Jerusalem, Israel

    Rina Fraenkel, Inbar Cahana, Noam Deouell & Netanel Tzarum

  4. Institute of Food Science and Biotechnology, Department of Food Microbiology, University of Hohenheim, Stuttgart, Germany

    Katharina Detert & Herbert Schmidt

  5. Department of Materials and Interfaces, Weizmann Institute of Science, Rehovot, Israel

    Monika Kluzek & Jacob Klein

  6. Department of Brain Sciences, Weizmann Institute of Science, Rehovot, Israel

    Sonu Peedikayil-Kurien & Meital Oren-Suissa

  7. Department of Molecular Neuroscience, Weizmann Institute of Science, Rehovot, Israel

    Sonu Peedikayil-Kurien & Meital Oren-Suissa

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  1. Nimrod Nachmias
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Contributions

A.L. conceived of and designed the study, managed the project and wrote the manuscript. N.N. performed the computational structural analysis, bacteriology and fungal and macrophage assays and wrote the paper. N. Dotan performed the computational analysis. M.C.R. performed the experiments with fungi. R.F. performed the biochemistry and structural analysis. K.D. constructed the knockouts in E. coli strain 48. M.K. performed the LUV experiments. M.S. performed some of the toxicity assays in E. coli. S.C., A.R. and N.S.-H. performed some of the computational analyses. S.P.-K. performed the experiments with nematodes. G.M. performed the experiments with moths. I.C. and N. Deouell helped with the structural and biochemical analyses. J.K., M.O.-S. and H.S. helped to write the manuscript. N.S. and N.T. designed the experiments in mycology and structural biology, respectively, performed data analysis and wrote the manuscript. Y.O.-S. designed and performed the experiments with bacteria and fungi, was responsible for most of the microscopy and wrote the manuscript.

Corresponding author

Correspondence to Asaf Levy.

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Extended data

Extended Data Fig. 1 Cell lysates of PT expressing E. coli inhibit fungal growth.

Antifungal activity of the toxins PT1Em (a), PT2Nm (b), PT3Rs (c), PT7Bc (d), PT8Li (e), and PT9Cn (f) against the fungi (left to right in each panel) A. fumigatus, A. nidulans, C. albicans, C. auris, C. Neoformans, and F. oxysporum. To determine the effect of PTs on fungal growth the indicator Alamar blue Fluorescence intensities (FI) of treated and untreated samples for each strain were obtained after 48 h of incubation. FI were used to calculate the percentage of toxicity. The fungal strains were grown with lysates of PTs expressing E. coli cells. Ctr; control of lysates of E. coli cells with an empty vector. NT, No treatment (on y axis).

Extended Data Fig. 2 PTs lead to cell death in various manners.

E. coli BL21 (DE3) cells harboring toxin genes (PT) or an empty vector control (Ctr) were grown in LB media in conditions that induce expression (0.2% arabinose). After 40 min of incubation, samples were stained with membrane and DNA stains and visualized by fluorescence microscopy. DNA (DAPI, blue), membrane (FM 1-43; green), and overlay images of the bacterial cells with toxins are presented. Arrows point to abnormal cells; PT3Rs: compressed chromosomes, PT4Ka: membrane disintegration and swollen cells, PT7Bc: missing DNA and membrane movement to the poles, PT8Li: abnormal shaped E. coli. Representative images from a single replicate out of three independent replicates are shown. Scale bar corresponds to 2 µm. Number of cells analyzed: PT1Em n = 1469, PT2Nm n = 1680, PT3Rs n = 1276, PT4Ka n = 1245, PT5Rb n = 1515, PT6Mc n = 1285, PT7B n = 1809, PT8Li n = 1564, PT9Cn n = 1381.

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Supplementary Tables list and Supplementary Figs. 1–15.

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Supplementary Tables 1–13.

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Nachmias, N., Dotan, N., Rocha, M.C. et al. Systematic discovery of antibacterial and antifungal bacterial toxins. Nat Microbiol 9, 3041–3058 (2024). https://doi.org/10.1038/s41564-024-01820-9

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