The type VI secretion system deploys antifungal effectors against microbial competitors

Katharina Trunk, Julien Peltier, Yi-Chia Liu, Brian D. Dill, Louise Walker, Neil A. R. Gow, Michael J. R. Stark, Janet Quinn, Henrik Strahl, Matthias Trost, Sarah J. Coulthurst

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Abstract

Interactions between bacterial and fungal cells shape many polymicrobial communities. Bacteria elaborate diverse strategies to interact and compete with other organisms, including the deployment of protein secretion systems. The type VI secretion system (T6SS) delivers toxic effector proteins into host eukaryotic cells and competitor bacterial cells, but, surprisingly, T6SS-delivered effectors targeting fungal cells have not been reported. Here we show that the ‘antibacterial’ T6SS of Serratia marcescens can act against fungal cells, including pathogenic Candida species, and identify the previously undescribed effector proteins responsible. These antifungal effectors, Tfe1 and Tfe2, have distinct impacts on the target cell, but both can ultimately cause fungal cell death. ‘In competition’ proteomics analysis revealed that T6SS-mediated delivery of Tfe2 disrupts nutrient uptake and amino acid metabolism in fungal cells, and leads to the induction of autophagy. Intoxication by Tfe1, in contrast, causes a loss of plasma membrane potential. Our findings extend the repertoire of the T6SS and suggest that antifungal T6SSs represent widespread and important determinants of the outcome of bacterial–fungal interactions.
Original languageEnglish
Pages (from-to)920-931
Number of pages12
JournalNature Microbiology
Volume3
Issue number8
Early online date23 Jul 2018
DOIs
Publication statusPublished - 1 Aug 2018

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Serratia marcescens
Cell Shape
Poisons
Autophagy
Eukaryotic Cells
Candida
Membrane Potentials
Proteomics
Proteins
Cell Death
Cell Membrane
Type VI Secretion Systems
Bacteria
Amino Acids
Protein Translocation Systems

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The type VI secretion system deploys antifungal effectors against microbial competitors. / Trunk, Katharina; Peltier, Julien; Liu, Yi-Chia; Dill, Brian D.; Walker, Louise; Gow, Neil A. R.; Stark, Michael J. R.; Quinn, Janet; Strahl, Henrik; Trost, Matthias; Coulthurst, Sarah J.

In: Nature Microbiology, Vol. 3, No. 8, 01.08.2018, p. 920-931.

Research output: Contribution to journalArticle

Trunk, K, Peltier, J, Liu, Y-C, Dill, BD, Walker, L, Gow, NAR, Stark, MJR, Quinn, J, Strahl, H, Trost, M & Coulthurst, SJ 2018, 'The type VI secretion system deploys antifungal effectors against microbial competitors', Nature Microbiology, vol. 3, no. 8, pp. 920-931. https://doi.org/10.1038/s41564-018-0191-x
Trunk, Katharina ; Peltier, Julien ; Liu, Yi-Chia ; Dill, Brian D. ; Walker, Louise ; Gow, Neil A. R. ; Stark, Michael J. R. ; Quinn, Janet ; Strahl, Henrik ; Trost, Matthias ; Coulthurst, Sarah J. / The type VI secretion system deploys antifungal effectors against microbial competitors. In: Nature Microbiology. 2018 ; Vol. 3, No. 8. pp. 920-931.
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abstract = "Interactions between bacterial and fungal cells shape many polymicrobial communities. Bacteria elaborate diverse strategies to interact and compete with other organisms, including the deployment of protein secretion systems. The type VI secretion system (T6SS) delivers toxic effector proteins into host eukaryotic cells and competitor bacterial cells, but, surprisingly, T6SS-delivered effectors targeting fungal cells have not been reported. Here we show that the ‘antibacterial’ T6SS of Serratia marcescens can act against fungal cells, including pathogenic Candida species, and identify the previously undescribed effector proteins responsible. These antifungal effectors, Tfe1 and Tfe2, have distinct impacts on the target cell, but both can ultimately cause fungal cell death. ‘In competition’ proteomics analysis revealed that T6SS-mediated delivery of Tfe2 disrupts nutrient uptake and amino acid metabolism in fungal cells, and leads to the induction of autophagy. Intoxication by Tfe1, in contrast, causes a loss of plasma membrane potential. Our findings extend the repertoire of the T6SS and suggest that antifungal T6SSs represent widespread and important determinants of the outcome of bacterial–fungal interactions.",
author = "Katharina Trunk and Julien Peltier and Yi-Chia Liu and Dill, {Brian D.} and Louise Walker and Gow, {Neil A. R.} and Stark, {Michael J. R.} and Janet Quinn and Henrik Strahl and Matthias Trost and Coulthurst, {Sarah J.}",
note = "This work was supported by the Wellcome Trust (Senior Research Fellowship in Basic Biomedical Science to S.J.C., 104556; 097377, J.Q.; 101873 & 200208, N.A.R.G.), the MRC (MR/K000111X/1, S.J .C; MC_UU_12016/5, M.T.), and the BBSRC (BB/K016393/1 & BB/P020119/1, J.Q.). We thank Maximilian Fritsch, Mario L{\'o}pez Mart{\'i}n and Birte Hollmann for help with strain construction; Gary Eitzen for construction of pGED1; Donna MacCallum for the gift of Candida glabrata ATCC2001; Joachim Morschh{\"a}user for the gift of pNIM1; Gillian Milne (Microscopy and Histology facility, University of Aberdeen) for assistance with TEM; and Peter Taylor, Michael Porter, Laura Monlezun and Colin Rickman for advice and technical assistance.",
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