Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling

Kening Zhao; Mark Bleackley; David Chisanga; Lahiru Gangoda; Pamali Fonseka; Michael Liem; Hina Kalra; Haidar Al Saffar; Shivakumar Keerthikumar; Ching-Seng Ang; Christopher G. Adda; Lanzhou Jiang; Kuok Yap; Ivan K. Poon; Peter Lock; Vincent Bulone; Marilyn Anderson; Suresh Mathivanan

doi:10.1038/s42003-019-0538-8

Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling

Kening Zhao, Mark Bleackley, David Chisanga, Lahiru Gangoda, Pamali Fonseka, Michael Liem, Hina Kalra, Haidar Al Saffar, Shivakumar Keerthikumar, Ching-Seng Ang, Christopher G. Adda, Lanzhou Jiang, Kuok Yap, Ivan K. Poon, Peter Lock, Vincent Bulone, Marilyn Anderson, Suresh Mathivanan

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Abstract

Extracellular vesicles (EVs) are membranous vesicles that are released by cells. In this study, the role of the Endosomal Sorting Complex Required for Transport (ESCRT) machinery in the biogenesis of yeast EVs was examined. Knockout of components of the ESCRT machinery altered the morphology and size of EVs as well as decreased the abundance of EVs. In contrast, strains with deletions in cell wall biosynthesis genes, produced more EVs than wildtype. Proteomic analysis highlighted the depletion of ESCRT components and enrichment of cell wall remodelling enzymes, glucan synthase subunit Fks1 and chitin synthase Chs3, in yeast EVs. Interestingly, EVs containing Fks1 and Chs3 rescued the yeast cells from antifungal molecules. However, EVs from fks1∆ or chs3∆ or the vps23∆chs3∆ double knockout strain were unable to rescue the yeast cells as compared to vps23∆ EVs. Overall, we have identified a potential role for yeast EVs in cell wall remodelling.

Original language	English
Article number	305
Number of pages	13
Journal	Communications Biology
Volume	2
DOIs	https://doi.org/10.1038/s42003-019-0538-8
Publication status	Published - 9 Aug 2019
Externally published	Yes

Bibliographical note

Funding Information:
Suresh Mathivanan is supported by Australian Research Council DECRA (DE150101777), Australian Research Council Discovery Project (DP170102312) and Australian Research Council Future Fellowship (FT180100333). Australian Research Council Discovery Project (DP160100309) supports the work of M.B., M.A. and V.B. Electron and optical microscopy presented in this study was performed in the LIMS Bioimaging Facility. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Confocal microscopy was performed in the LIMS BioImaging facility.

Publisher Copyright:
© 2019, The Author(s).

Keywords

Extracellular vesicles
EVs
membranous vesicles
cells
Endosomal Sorting Complex Required for Transport
ESCRT
ESCRT machinery
morphology
antifungal molecules
Saccharomyces cerevisiae
cell wall remodelling

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Zhao, K., Bleackley, M., Chisanga, D., Gangoda, L., Fonseka, P., Liem, M., Kalra, H., Al Saffar, H., Keerthikumar, S., Ang, C.-S., Adda, C. G., Jiang, L., Yap, K., Poon, I. K., Lock, P., Bulone, V., Anderson, M., & Mathivanan, S. (2019). Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling. Communications Biology, 2, Article 305. https://doi.org/10.1038/s42003-019-0538-8

@article{a6b7643633514349a94b54a9f3ab0999,

title = "Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling",

abstract = "Extracellular vesicles (EVs) are membranous vesicles that are released by cells. In this study, the role of the Endosomal Sorting Complex Required for Transport (ESCRT) machinery in the biogenesis of yeast EVs was examined. Knockout of components of the ESCRT machinery altered the morphology and size of EVs as well as decreased the abundance of EVs. In contrast, strains with deletions in cell wall biosynthesis genes, produced more EVs than wildtype. Proteomic analysis highlighted the depletion of ESCRT components and enrichment of cell wall remodelling enzymes, glucan synthase subunit Fks1 and chitin synthase Chs3, in yeast EVs. Interestingly, EVs containing Fks1 and Chs3 rescued the yeast cells from antifungal molecules. However, EVs from fks1∆ or chs3∆ or the vps23∆chs3∆ double knockout strain were unable to rescue the yeast cells as compared to vps23∆ EVs. Overall, we have identified a potential role for yeast EVs in cell wall remodelling.",

keywords = "Extracellular vesicles, EVs, membranous vesicles, cells, Endosomal Sorting Complex Required for Transport, ESCRT, ESCRT machinery, morphology, antifungal molecules, Saccharomyces cerevisiae, cell wall remodelling",

author = "Kening Zhao and Mark Bleackley and David Chisanga and Lahiru Gangoda and Pamali Fonseka and Michael Liem and Hina Kalra and {Al Saffar}, Haidar and Shivakumar Keerthikumar and Ching-Seng Ang and Adda, {Christopher G.} and Lanzhou Jiang and Kuok Yap and Poon, {Ivan K.} and Peter Lock and Vincent Bulone and Marilyn Anderson and Suresh Mathivanan",

note = "Funding Information: Suresh Mathivanan is supported by Australian Research Council DECRA (DE150101777), Australian Research Council Discovery Project (DP170102312) and Australian Research Council Future Fellowship (FT180100333). Australian Research Council Discovery Project (DP160100309) supports the work of M.B., M.A. and V.B. Electron and optical microscopy presented in this study was performed in the LIMS Bioimaging Facility. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Confocal microscopy was performed in the LIMS BioImaging facility. Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = aug,

day = "9",

doi = "10.1038/s42003-019-0538-8",

language = "English",

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Zhao, K, Bleackley, M, Chisanga, D, Gangoda, L, Fonseka, P, Liem, M, Kalra, H, Al Saffar, H, Keerthikumar, S, Ang, C-S, Adda, CG, Jiang, L, Yap, K, Poon, IK, Lock, P, Bulone, V, Anderson, M & Mathivanan, S 2019, 'Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling', Communications Biology, vol. 2, 305. https://doi.org/10.1038/s42003-019-0538-8

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AU - Zhao, Kening

AU - Bleackley, Mark

AU - Chisanga, David

AU - Gangoda, Lahiru

AU - Fonseka, Pamali

AU - Liem, Michael

AU - Kalra, Hina

AU - Al Saffar, Haidar

AU - Keerthikumar, Shivakumar

AU - Ang, Ching-Seng

AU - Adda, Christopher G.

AU - Jiang, Lanzhou

AU - Yap, Kuok

AU - Poon, Ivan K.

AU - Lock, Peter

AU - Bulone, Vincent

AU - Anderson, Marilyn

AU - Mathivanan, Suresh

N1 - Funding Information: Suresh Mathivanan is supported by Australian Research Council DECRA (DE150101777), Australian Research Council Discovery Project (DP170102312) and Australian Research Council Future Fellowship (FT180100333). Australian Research Council Discovery Project (DP160100309) supports the work of M.B., M.A. and V.B. Electron and optical microscopy presented in this study was performed in the LIMS Bioimaging Facility. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Confocal microscopy was performed in the LIMS BioImaging facility. Publisher Copyright: © 2019, The Author(s).

PY - 2019/8/9

Y1 - 2019/8/9

N2 - Extracellular vesicles (EVs) are membranous vesicles that are released by cells. In this study, the role of the Endosomal Sorting Complex Required for Transport (ESCRT) machinery in the biogenesis of yeast EVs was examined. Knockout of components of the ESCRT machinery altered the morphology and size of EVs as well as decreased the abundance of EVs. In contrast, strains with deletions in cell wall biosynthesis genes, produced more EVs than wildtype. Proteomic analysis highlighted the depletion of ESCRT components and enrichment of cell wall remodelling enzymes, glucan synthase subunit Fks1 and chitin synthase Chs3, in yeast EVs. Interestingly, EVs containing Fks1 and Chs3 rescued the yeast cells from antifungal molecules. However, EVs from fks1∆ or chs3∆ or the vps23∆chs3∆ double knockout strain were unable to rescue the yeast cells as compared to vps23∆ EVs. Overall, we have identified a potential role for yeast EVs in cell wall remodelling.

AB - Extracellular vesicles (EVs) are membranous vesicles that are released by cells. In this study, the role of the Endosomal Sorting Complex Required for Transport (ESCRT) machinery in the biogenesis of yeast EVs was examined. Knockout of components of the ESCRT machinery altered the morphology and size of EVs as well as decreased the abundance of EVs. In contrast, strains with deletions in cell wall biosynthesis genes, produced more EVs than wildtype. Proteomic analysis highlighted the depletion of ESCRT components and enrichment of cell wall remodelling enzymes, glucan synthase subunit Fks1 and chitin synthase Chs3, in yeast EVs. Interestingly, EVs containing Fks1 and Chs3 rescued the yeast cells from antifungal molecules. However, EVs from fks1∆ or chs3∆ or the vps23∆chs3∆ double knockout strain were unable to rescue the yeast cells as compared to vps23∆ EVs. Overall, we have identified a potential role for yeast EVs in cell wall remodelling.

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KW - cells

KW - Endosomal Sorting Complex Required for Transport

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KW - ESCRT machinery

KW - morphology

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KW - Saccharomyces cerevisiae

KW - cell wall remodelling

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AN - SCOPUS:85071178113

SN - 2399-3642

VL - 2

JO - Communications Biology

JF - Communications Biology

M1 - 305

ER -

Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling

Abstract

Bibliographical note

Keywords

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