Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin

Abstract Formation and breakage of disulfide bridges strongly impacts folding and activity of proteins. Thioredoxin 1 (TrxA) is a small, conserved enzyme that reduces disulfide bonds in the bacterial cytosol. In this study, we provide an example of the emergence of a chaperone role for TrxA, which i...

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Main Authors: Baptiste Dumont, Laurent Terradot, Eric Cascales, Laurence Van Melderen, Dukas Jurėnas
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54892-w
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author Baptiste Dumont
Laurent Terradot
Eric Cascales
Laurence Van Melderen
Dukas Jurėnas
author_facet Baptiste Dumont
Laurent Terradot
Eric Cascales
Laurence Van Melderen
Dukas Jurėnas
author_sort Baptiste Dumont
collection DOAJ
description Abstract Formation and breakage of disulfide bridges strongly impacts folding and activity of proteins. Thioredoxin 1 (TrxA) is a small, conserved enzyme that reduces disulfide bonds in the bacterial cytosol. In this study, we provide an example of the emergence of a chaperone role for TrxA, which is independent of redox catalysis. We show that the activity of the secreted bacterial ADP-ribosyltransferase (ART) toxin TreX, which does not contain any cysteines, is dependent on TrxA. TreX binds to the reduced form of TrxA via its carboxy-terminal extension to form a soluble and active complex. Structural studies revealed that TreX-like toxins are homologous to Scabin-like ART toxins which possess cysteine residues and form disulfide bridges at the position that superimposes the TrxA binding site in TreX. Our study therefore suggests that thioredoxin 1 evolved alternative functions by maintaining the interaction with cysteine-free substrates.
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spelling doaj-art-afead9ac7c6c4a9d9c7b7c15f4e0e4a62024-12-01T12:33:45ZengNature PortfolioNature Communications2041-17232024-11-0115111510.1038/s41467-024-54892-wThioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxinBaptiste Dumont0Laurent Terradot1Eric Cascales2Laurence Van Melderen3Dukas Jurėnas4Bacterial Genetics and Physiology, Faculté des Sciences, Université Libre de Bruxelles (ULB)Laboratory of Molecular Microbiology and Structural Biochemistry, Institut de Biologie et Chimie des Protéines (IBCP), Université de LyonLaboratoire d’Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie de la Méditerranée (IMM), Aix-Marseille UniversitéBacterial Genetics and Physiology, Faculté des Sciences, Université Libre de Bruxelles (ULB)Bacterial Genetics and Physiology, Faculté des Sciences, Université Libre de Bruxelles (ULB)Abstract Formation and breakage of disulfide bridges strongly impacts folding and activity of proteins. Thioredoxin 1 (TrxA) is a small, conserved enzyme that reduces disulfide bonds in the bacterial cytosol. In this study, we provide an example of the emergence of a chaperone role for TrxA, which is independent of redox catalysis. We show that the activity of the secreted bacterial ADP-ribosyltransferase (ART) toxin TreX, which does not contain any cysteines, is dependent on TrxA. TreX binds to the reduced form of TrxA via its carboxy-terminal extension to form a soluble and active complex. Structural studies revealed that TreX-like toxins are homologous to Scabin-like ART toxins which possess cysteine residues and form disulfide bridges at the position that superimposes the TrxA binding site in TreX. Our study therefore suggests that thioredoxin 1 evolved alternative functions by maintaining the interaction with cysteine-free substrates.https://doi.org/10.1038/s41467-024-54892-w
spellingShingle Baptiste Dumont
Laurent Terradot
Eric Cascales
Laurence Van Melderen
Dukas Jurėnas
Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin
Nature Communications
title Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin
title_full Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin
title_fullStr Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin
title_full_unstemmed Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin
title_short Thioredoxin 1 moonlights as a chaperone for an interbacterial ADP-ribosyltransferase toxin
title_sort thioredoxin 1 moonlights as a chaperone for an interbacterial adp ribosyltransferase toxin
url https://doi.org/10.1038/s41467-024-54892-w
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