Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of Saccharomyces cerevisiae to stress induced by sulfur dioxide

Authors:

Patrícia Lage1,2, Belém Sampaio-Marques3,4, Paula Ludovico3,4, Nuno P. Mira5 and Ana Mendes-Ferreira1,2

doi: 10.15698/mic2019.11.697
Volume 6, pp. 509 to 523, published 30/09/2019.

PDF Download PubMed Link Supplemental Information
Affiliations:

1 Universidade de Trás-os-Montes e Alto Douro, Escola de Ciências da Vida e Ambiente; Vila Real, Portugal.

2 BioISI – Biosystems & Integrative Sciences Institute, Campo Grande, Lisboa, Portugal.

3 Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, 4710-057 Braga, Portugal.

4 ICVS/3B’s – PT Government Associate Laboratory, Braga/Guimarães, Portugal.

5 Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Department of Bioengineering, University of Lisbon, Portugal.

Keywords: 

Sulfur dioxide tolerance, Com2 (YER130c), wine preservation, Saccharomyces cerevisiae, stress response.

Corresponding Author(s):

Ana Mendes-Ferreira, , BioISI - Universidade de Trás-os-Montes e Alto Douro, Escola de Ciências da Vida e Ambiente; Vila Real, Portugal; anamf@utad.pt Nuno P Mira, Instituto Superior Técnico, Department of Bioengineering, University of Lisbon, Portugal; nuno.mira@tecnico.ulisboa.pt

Conflict of interest statement:

The authors declare no conflict of interest.

Please cite this article as:

Patrícia Lage, Belém Sampaio-Marques, Paula Ludovico, Nuno P Mira and Ana Mendes-Ferreira (2019). Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of Saccharomyces cere-visiae to stress induced by sulfur dioxide. Microbial Cell 6(11): 509-523. doi: 10.15698/mic2019.11.697

© 2019 Lage et al. This is an open-access article released under the terms of the Creative Commons Attribution (CC BY) license, which allows the unrestricted use, distribution, and reproduc-tion in any medium, provided the original author and source are acknowledged.

Abstract:

During vinification Saccharomyces cerevisiae cells are frequently exposed to high concentrations of sulfur dioxide (SO2) that is used to avoid overgrowth of unwanted bacteria or fungi present in the must. Up to now the characterization of the molecular mechanisms by which S. cerevisiae responds and tolerates SO2 was focused on the role of the sulfite efflux pump Ssu1 and investigation on the involvement of other players has been scarce, especially at a genome-wide level. In this work, we uncovered the essential role of the poorly characterized transcription factor Com2 in tolerance and response of S. cerevisiae to stress induced by SO2 at the enologically relevant pH of 3.5. Transcriptomic analysis revealed that Com2 controls, directly or indirectly, the expression of more than 80% of the genes activated by SO2, a percentage much higher than the one that could be attributed to any other stress-responsive transcription factor. Large-scale phenotyping of the yeast haploid mutant collection led to the identification of 50 Com2-targets contributing to the protection against SO2 including all the genes that compose the sulfate reduction pathway (MET3, MET14, MET16, MET5, MET10) and the majority of the genes required for biosynthesis of lysine (LYS2, LYS21, LYS20, LYS14, LYS4, LYS5, LYS1 and LYS9) or arginine (ARG5,6, ARG4, ARG2, ARG3, ARG7, ARG8, ORT1 and CPA1). Other uncovered determinants of resistance to SO2 (not under the control of Com2) included genes required for function and assembly of the vacuolar proton pump and enzymes of the antioxidant defense, consistent with the observed cytosolic and mitochondrial accumulation of reactive oxygen species in SO2-stressed yeast cells.