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[Preprint]. 2024 Dec 18:2024.09.27.615498. [Version 2] doi: 10.1101/2024.09.27.615498

Identification of novel toxin domains and characterization of a broadly distributed family of lipid-targeting NlpC/P60

Gianlucca G Nicastro, Stephanie Sibinelli-Sousa, Julia Takuno Hespanhol, Thomas W C Santos, Joseph P Munoz, Rosangela S Santos, Blanca M Perez-Sepulveda, Sayuri Miyamoto, L Aravind, Robson F de Souza, Ethel Bayer-Santos
PMCID: PMC11996579  PMID: 40236209

Abstract

Bacterial warfare is a common and ancient phenomenon in nature, where bacterial species use strategies to inhibit the growth or kill competitors. This involves the production and deployment of antibacterial toxins that disrupt essential cellular processes in target cells. Polymorphic toxins comprise a group of offensive systems with a modular structure featuring a conserved N-terminal translocation domain fused to diverse C-terminal toxin domains. The continuous arms race in which bacteria acquire new toxin and immunity proteins to promote increased adaptation to their environment is responsible for the diversification of this toxin repertoire. Here, we deployed in-silico strategies to analyze 10,000 genomes and identify toxin domains secreted via the type VI secretion system of Salmonella . We identified and manually curated 128 candidates, which are widespread polymorphic toxins detected in a vast array of species and linked to diverse secretion systems. In addition, 45 previously uncharacterized toxin domains were identified. STox15 was among the most frequent candidates found in the dataset and was selected for in-depth characterization. STox15 is an antibacterial effector belonging to the NlpC/P60 papain-like fold superfamily with a permuted catalytic core typical of lipid-targeting versions rather than peptidases or amidases. Biochemical analysis with recombinant protein and lipidomics of intoxicated Escherichia coli revealed that STox15 displays phospholipase activity cleaving off acyl groups from phosphatidylglycerol and phosphatidylethanolamine.

Importance

This work broadens our understanding of polymorphic toxin domains and provides the first direct characterization of a lipid-targeting NlpC/P60 domain in biological conflicts.

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