Role of Saccharomyces cerevisiae Nutrient Signaling Pathways During Winemaking: A Phenomics Approach.

Beatriz Vallejo,Victor Garrigós,Agustín Aranda,Emilien Peltier,Emilia Matallana,Philippe Marullo

doi:10.3389/fbioe.2020.00853

Abstract

The ability of the yeast Saccharomyces cerevisiae to adapt to the changing environment of industrial processes lies in the activation and coordination of many molecular pathways. The most relevant ones are nutrient signaling pathways because they control growth and stress response mechanisms as a result of nutrient availability or scarcity and, therefore, leave an ample margin to improve yeast biotechnological performance. A standardized grape juice fermentation assay allowed the analysis of mutants for different elements of many nutrient signaling pathways under different conditions (low/high nitrogen and different oxygenation levels) to allow genetic-environment interactions to be analyzed. The results indicate that the cAMP-dependent PKA pathway is the most relevant regardless of fermentation conditions, while mutations on TOR pathways display an effect that depends on nitrogen availability. The production of metabolites of interest, such as glycerol, acetic acid and pyruvate, is controlled in a coordinated manner by the contribution of several components of different pathways. Ras GTPase Ras2, a stimulator of cAMP production, is a key factor for achieving fermentation, and is also relevant for sensing nitrogen availability. Increasing cAMP concentrations by deleting an enzyme used for its degradation, phosphodiesterase Pde2, proved a good way to increase fermentation kinetics, and offered keys for biotechnological improvement. Surprisingly glucose repression protein kinase Snf1 and Nitrogen Catabolite Repression transcription factor Gln3 are relevant in fermentation, even in the absence of starvation. Gln3 proved essential for respiration in several genetic backgrounds, and its presence is required to achieve full glucose de-repression. Therefore, most pathways sense different types of nutrients and only their coordinated action can ensure successful wine fermentation.

Highlights

Saccharomyces cerevisiae has been used as a very successful model organism to explain the molecular mechanisms regulating cell growth and metabolism (Conrad et al, 2014; Rodkaer and Faergeman, 2014; Zhang et al, 2018)
Our results indicate that nutrient signaling pathway genetic manipulation can be a good target of performance improvement
The used genetic background was a haploid derivative of wine commercial strain L2056 called C9, which is a convenient background for performing gene deletions (Walker et al, 2005)

Summary

Introduction

Saccharomyces cerevisiae has been used as a very successful model organism to explain the molecular mechanisms regulating cell growth and metabolism (Conrad et al, 2014; Rodkaer and Faergeman, 2014; Zhang et al, 2018). In the presence of glucose, which is a principal carbon source of laboratory media, cAMP-dependent protein kinase A (PKA) represses the stress response and stimulates fermentation and cell proliferation (Conrad et al, 2014). NCR is activated by good nitrogen sources like ammonia and glutamine, and is repressed by poor sources like proline. This system contains two transcription factors, Gln and Gat, and one repressor protein, Ure. In addition to TORC1, and regarding amino acid signaling, the General Amino Acid Control kinase Gcn senses amino acid starvation to promote the biosynthesis of nitrogen compounds through transcription factor Gcn (Conrad et al, 2014)

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