Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex

Abstract

The type VI secretion system (T6SS) is a multiprotein machine widespread in Gram-negative bacteria that delivers toxins into both eukaryotic and prokaryotic cells. The mechanism of action of the T6SS is comparable to that of contractile myophages. The T6SS builds a tail-like structure made of an inner tube wrapped by a sheath, assembled under an extended conformation. Contraction of the sheath propels the inner tube towards the target cell. The T6SS tail is assembled on a platform—the baseplate—which is functionally similar to bacteriophage baseplates. In addition, the baseplate docks the tail to a trans-envelope membrane complex that orients the tail towards the target. Here, we report the crystal structure of TssK, a central component of the T6SS baseplate. We show that TssK is composed of three domains, and establish the contribution of each domain to the interaction with TssK partners. Importantly, this study reveals that the N-terminal domain of TssK is structurally homologous to the shoulder domain of phage receptor-binding proteins, and the C-terminal domain binds the membrane complex. We propose that TssK has conserved the domain of attachment to the virion particle but has evolved the reception domain to use the T6SS membrane complex as receptor.

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Figure 1: Structure of TssK.
Figure 2: Structure of the TssKSN–nbK18–nbK27 complex.
Figure 3: Structural comparison of the TssK N-terminal shoulder domain with shoulder domains of siphophage RBPs.
Figure 4: Protein–protein interaction study of TssK domains.
Figure 5: Schematic model of the baseplate docked to the membrane complex, highlighting the connector role of TssK.

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Acknowledgements

The authors thank the members of the Cambillau/Roussel and Cascales laboratories for discussions, A. Kassa for initial work on TssK, L. Journet for critical reading of the manuscript, the Soleil (Saint Aubin, France) and ESRF (Grenoble, France) synchrotrons for beam time allocation and A. Brun, I. Bringer and O. Uderso for technical assistance. This work was supported by the Centre National de la Recherche Scientifique and the Aix-Marseille Université and grants from the Agence Nationale de la Recherche (ANR-14-CE14-0006-02) and the French Infrastructure for Integrated Structural Biology (FRISBI). V.S.N. was supported by a fellowship from the French Embassy in Vietnam. L.L. and A.Z. were supported by doctoral fellowships of the Ministère Français de l'Enseignement Supérieur et de la Recherche and end-of-thesis fellowships from the Fondation pour la Recherche Médicale (FRM) (FDT20160435498 and FDT20140931060, respectively). T.T.N.T. was supported by a grant from the Ministère des Affaires Etrangères, France (no. 861733C). Y.C. is supported by a doctoral school PhD fellowship from the FRM (ECO20160736014).

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V.S.N., E.C. and C.C. designed the study. V.S.N., L.L., S.S., P.L., T.T.H.P., T.T.N.T., Y.C., A.Z., A.D., E.D., A.R., C.K., E.C. and C.C. contributed to analysis of the data and preparation of this manuscript. V.S.N., S.S., P.L. and C.C. perform the protein production, crystallization and crystallographic experiments. T.T.H.P. and T.T.N.T. contributed to protein production and crystallization. A.D. performed nanobodies selection and characterization. E.D. provided the TssKFG clone. C.K. performed the BLI and HPLC experiments. L.L., Y.C., A.Z. and E.C performed the double hybrid and co-immunoprecipitation experiments.

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Correspondence to Eric Cascales or Christian Cambillau.

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Nguyen, V., Logger, L., Spinelli, S. et al. Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex. Nat Microbiol 2, 17103 (2017). https://doi.org/10.1038/nmicrobiol.2017.103

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