Adaptive response to chronic mild ethanol stress involves ROS, sirtuins and changes in chromosome dosage in wine yeasts.

Jagoda Adamczyk,Leszek Potocki,Anna Lewinska,Maciej Wnuk,Anna Deregowska,Adrianna Skoneczna,Jakub Kaplan,Ewa Rawska,Aleksandra Kwiatkowska,Marek Skoneczny,Sylwia Pabian

doi:10.18632/oncotarget.8673

Abstract

Industrial yeast strains of economic importance used in winemaking and beer production are genomically diverse and subjected to harsh environmental conditions during fermentation. In the present study, we investigated wine yeast adaptation to chronic mild alcohol stress when cells were cultured for 100 generations in the presence of non-cytotoxic ethanol concentration. Ethanol-induced reactive oxygen species (ROS) and superoxide signals promoted growth rate during passages that was accompanied by increased expression of sirtuin proteins, Sir1, Sir2 and Sir3, and DNA-binding transcription regulator Rap1. Genome-wide array-CGH analysis revealed that yeast genome was shaped during passages. The gains of chromosomes I, III and VI and significant changes in the gene copy number in nine functional gene categories involved in metabolic processes and stress responses were observed. Ethanol-mediated gains of YRF1 and CUP1 genes were the most accented. Ethanol also induced nucleolus fragmentation that confirms that nucleolus is a stress sensor in yeasts. Taken together, we postulate that wine yeasts of different origin may adapt to mild alcohol stress by shifts in intracellular redox state promoting growth capacity, upregulation of key regulators of longevity, namely sirtuins and changes in the dosage of genes involved in the telomere maintenance and ion detoxification.

Highlights

Ethanol stress is one of the major environmental stresses generated during microbe-based industrial fermentations, e.g., beer production or winemaking that may affect their performance [1, 2]
We found that chronic mild ethanol stress induced reactive oxygen species (ROS) and superoxide signaling and the upregulation of sirtuin proteins that promoted cell growth during passages
It has been reported that hydrogen peroxide extended chronological lifespan in the budding yeast as a response to caloric restriction or inactivation of catalases and in cells exposed to low levels of hydrogen peroxide [32]

Summary

Introduction

Ethanol stress is one of the major environmental stresses generated during microbe-based industrial fermentations, e.g., beer production or winemaking that may affect their performance [1, 2]. The elucidation of the mechanisms of ethanol adaptive responses and tolerance in industrial yeast strains of Saccharomyces cerevisiae species is of fundamental scientific interest as well as of economic importance due to heavy demand for alternative energy sources, namely renewable biofuels such as ethanol [3]. As ethanol increases the fluidity and permeability of the plasma membrane affecting the functions of membrane proteins and cell transport that, in turn, may compromise yeast cell physiology, ethanol-induced cell response is primarily based on the changes in membrane composition preventing membrane fluidization and promoting its www.impactjournals.com/oncotarget No Trade name Portwein Bordeaux Tokay Tokay 22 Fermivin. Aromatic Wine Complex PDM Maurivin PRIMEUR Maurivin

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