Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1

The K1 A/B toxin secreted by virus-infected Saccharomyces cerevisiae strains kills sensitive cells via disturbance of cytoplasmic membrane functions. Despite decades of research, the mechanisms underlying K1 toxicity and immunity have not been elucidated yet. In a novel approach, this study aimed to...

Full description

Bibliographic Details
Main Authors: Stefanie Gier, Martin Simon, Karl Nordström, Salem Khalifa, Marcel H. Schulz, Manfred J. Schmitt, Frank Breinig
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01102/full
_version_ 1828396574070276096
author Stefanie Gier
Stefanie Gier
Martin Simon
Martin Simon
Martin Simon
Karl Nordström
Karl Nordström
Salem Khalifa
Marcel H. Schulz
Manfred J. Schmitt
Manfred J. Schmitt
Frank Breinig
Frank Breinig
author_facet Stefanie Gier
Stefanie Gier
Martin Simon
Martin Simon
Martin Simon
Karl Nordström
Karl Nordström
Salem Khalifa
Marcel H. Schulz
Manfred J. Schmitt
Manfred J. Schmitt
Frank Breinig
Frank Breinig
author_sort Stefanie Gier
collection DOAJ
description The K1 A/B toxin secreted by virus-infected Saccharomyces cerevisiae strains kills sensitive cells via disturbance of cytoplasmic membrane functions. Despite decades of research, the mechanisms underlying K1 toxicity and immunity have not been elucidated yet. In a novel approach, this study aimed to characterize transcriptome changes in K1-treated sensitive yeast cells in a time-dependent manner. Global transcriptional profiling revealed substantial cellular adaptations in target cells resulting in 1,189 differentially expressed genes in total. Killer toxin K1 induced oxidative, cell wall and hyperosmotic stress responses as well as rapid down-regulation of transcription and translation. Essential pathways regulating energy metabolism were also significantly affected by the toxin. Remarkably, a futile cycle of the osmolytes trehalose and glycogen was identified probably representing a critical feature of K1 intoxication. In silico analysis suggested several transcription factors involved in toxin-triggered signal transduction. The identified transcriptome changes provide valuable hints to illuminate the still unknown molecular events leading to K1 toxicity and immunity implicating an evolutionarily conserved response at least initially counteracting ionophoric toxin action.
first_indexed 2024-12-10T08:32:28Z
format Article
id doaj.art-5bf5710ba7c94952ac8e6ec0799237fa
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-10T08:32:28Z
publishDate 2019-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-5bf5710ba7c94952ac8e6ec0799237fa2022-12-22T01:56:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-05-011010.3389/fmicb.2019.01102444781Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1Stefanie Gier0Stefanie Gier1Martin Simon2Martin Simon3Martin Simon4Karl Nordström5Karl Nordström6Salem Khalifa7Marcel H. Schulz8Manfred J. Schmitt9Manfred J. Schmitt10Frank Breinig11Frank Breinig12Department of Molecular and Cell Biology, Saarland University, Saarbrücken, GermanyCenter of Human and Molecular Biology (ZHMB), Saarland University, Saarbrücken, GermanyCenter of Human and Molecular Biology (ZHMB), Saarland University, Saarbrücken, GermanyMolecular Cell Biology and Microbiology, University of Wuppertal, Wuppertal, GermanyMolecular Cell Dynamics, Saarland University, Saarbrücken, GermanyCenter of Human and Molecular Biology (ZHMB), Saarland University, Saarbrücken, GermanyDepartment of Genetics/Epigenetics, Saarland University, Saarbrücken, GermanyCluster of Excellence “Multimodal Computing and Interaction”, Max Planck Institute for Informatics, Saarland University, Saarbrücken, GermanyCluster of Excellence “Multimodal Computing and Interaction”, Max Planck Institute for Informatics, Saarland University, Saarbrücken, GermanyDepartment of Molecular and Cell Biology, Saarland University, Saarbrücken, GermanyCenter of Human and Molecular Biology (ZHMB), Saarland University, Saarbrücken, GermanyDepartment of Molecular and Cell Biology, Saarland University, Saarbrücken, GermanyCenter of Human and Molecular Biology (ZHMB), Saarland University, Saarbrücken, GermanyThe K1 A/B toxin secreted by virus-infected Saccharomyces cerevisiae strains kills sensitive cells via disturbance of cytoplasmic membrane functions. Despite decades of research, the mechanisms underlying K1 toxicity and immunity have not been elucidated yet. In a novel approach, this study aimed to characterize transcriptome changes in K1-treated sensitive yeast cells in a time-dependent manner. Global transcriptional profiling revealed substantial cellular adaptations in target cells resulting in 1,189 differentially expressed genes in total. Killer toxin K1 induced oxidative, cell wall and hyperosmotic stress responses as well as rapid down-regulation of transcription and translation. Essential pathways regulating energy metabolism were also significantly affected by the toxin. Remarkably, a futile cycle of the osmolytes trehalose and glycogen was identified probably representing a critical feature of K1 intoxication. In silico analysis suggested several transcription factors involved in toxin-triggered signal transduction. The identified transcriptome changes provide valuable hints to illuminate the still unknown molecular events leading to K1 toxicity and immunity implicating an evolutionarily conserved response at least initially counteracting ionophoric toxin action.https://www.frontiersin.org/article/10.3389/fmicb.2019.01102/fullK1killer toxinyeast viral toxinSaccharomyces cerevisiaetranscriptome
spellingShingle Stefanie Gier
Stefanie Gier
Martin Simon
Martin Simon
Martin Simon
Karl Nordström
Karl Nordström
Salem Khalifa
Marcel H. Schulz
Manfred J. Schmitt
Manfred J. Schmitt
Frank Breinig
Frank Breinig
Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1
Frontiers in Microbiology
K1
killer toxin
yeast viral toxin
Saccharomyces cerevisiae
transcriptome
title Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1
title_full Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1
title_fullStr Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1
title_full_unstemmed Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1
title_short Transcriptome Kinetics of Saccharomyces cerevisiae in Response to Viral Killer Toxin K1
title_sort transcriptome kinetics of saccharomyces cerevisiae in response to viral killer toxin k1
topic K1
killer toxin
yeast viral toxin
Saccharomyces cerevisiae
transcriptome
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01102/full
work_keys_str_mv AT stefaniegier transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT stefaniegier transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT martinsimon transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT martinsimon transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT martinsimon transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT karlnordstrom transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT karlnordstrom transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT salemkhalifa transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT marcelhschulz transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT manfredjschmitt transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT manfredjschmitt transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT frankbreinig transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1
AT frankbreinig transcriptomekineticsofsaccharomycescerevisiaeinresponsetoviralkillertoxink1