Specialized Listeria monocytogenes produce tailocins to provide a population-level competitive growth advantage

Nadejda Sigal; Rotem Lichtenstein-Wolfheim; Shai Schlussel; Gil Azulay; Ilya Borovok; Vered Holdengraber; Nadav Elad; Sharon G. Wolf; Ran Zalk; Raz Zarivach; Gabriel A. Frank; Anat A. Herskovits

doi:10.1038/s41564-024-01793-9

Specialized Listeria monocytogenes produce tailocins to provide a population-level competitive growth advantage

Nadejda Sigal, Rotem Lichtenstein-Wolfheim, Shai Schlussel, Gil Azulay, Ilya Borovok, Vered Holdengraber, Nadav Elad, Sharon G. Wolf, Ran Zalk, Raz Zarivach, Gabriel A. Frank, Anat A. Herskovits^*

^*Corresponding author for this work

Department of Chemical Research Support

Research output: Contribution to journal › Article › peer-review

Abstract

Tailocins are phage tail-like bacteriocins produced by various bacterial species to kill kin competitors. Given that tailocin release is dependent upon cell lysis, regulation of tailocin production at the single-cell and population level remains unclear. Here we used flow cytometry, competition assays and structural characterization of tailocin production in a human bacterial pathogen, Listeria monocytogenes. We revealed that a specialized subpopulation, constituting less than 1% of the total bacterial population, differentiates to produce, assemble and store thousands of tailocin particles. Tailocins are packed in a highly ordered manner, clustered in a liquid crystalline phase that occupies a substantial volume of the cell. Tailocin production confers a competitive growth advantage for the rest of the population. This study provides molecular insights into tailocin production as a form of altruism, showing how cell specialization within bacterial populations can confer competitive advantages at the population level.

Original language	English
Pages (from-to)	2727-2737
Number of pages	11
Journal	Nature Microbiology
Volume	9
Issue number	10
Early online date	19 Sept 2024
DOIs	https://doi.org/10.1038/s41564-024-01793-9
Publication status	Published - Oct 2024

Funding

This work was funded by an ERC Consolidator Grant (Co-Patho-phage, 817842) from the European Research Council awarded to A.A.H. and by Instruct-ERIC to A.A.H. via the Weizmann Institute of Science (PID 18811). The electron microscopy studies were partially supported by the Irving and Cherna Moskowitz Center for Nano and Bio-nano Imaging (Weizmann Institute of Science). Publisher Copyright: © The Author(s), under exclusive licence to Springer Nature Limited 2024.

All Science Journal Classification (ASJC) codes

Microbiology
Immunology
Applied Microbiology and Biotechnology
Genetics
Microbiology (medical)
Cell Biology

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10.1038/s41564-024-01793-9

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Sigal, N., Lichtenstein-Wolfheim, R., Schlussel, S., Azulay, G., Borovok, I., Holdengraber, V., Elad, N., Wolf, S. G., Zalk, R., Zarivach, R., Frank, G. A., & Herskovits, A. A. (2024). Specialized Listeria monocytogenes produce tailocins to provide a population-level competitive growth advantage. Nature Microbiology, 9(10), 2727-2737. https://doi.org/10.1038/s41564-024-01793-9

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abstract = "Tailocins are phage tail-like bacteriocins produced by various bacterial species to kill kin competitors. Given that tailocin release is dependent upon cell lysis, regulation of tailocin production at the single-cell and population level remains unclear. Here we used flow cytometry, competition assays and structural characterization of tailocin production in a human bacterial pathogen, Listeria monocytogenes. We revealed that a specialized subpopulation, constituting less than 1% of the total bacterial population, differentiates to produce, assemble and store thousands of tailocin particles. Tailocins are packed in a highly ordered manner, clustered in a liquid crystalline phase that occupies a substantial volume of the cell. Tailocin production confers a competitive growth advantage for the rest of the population. This study provides molecular insights into tailocin production as a form of altruism, showing how cell specialization within bacterial populations can confer competitive advantages at the population level.",

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Sigal, N, Lichtenstein-Wolfheim, R, Schlussel, S, Azulay, G, Borovok, I, Holdengraber, V, Elad, N , Wolf, SG, Zalk, R, Zarivach, R, Frank, GA & Herskovits, AA 2024, 'Specialized Listeria monocytogenes produce tailocins to provide a population-level competitive growth advantage', Nature Microbiology, vol. 9, no. 10, pp. 2727-2737. https://doi.org/10.1038/s41564-024-01793-9

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Specialized Listeria monocytogenes produce tailocins to provide a population-level competitive growth advantage

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