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...
Main Authors: | , , , , , , |
---|---|
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 |