International Journal of Molecular Sciences (Mar 2023)
Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i>
- Ivan Rodrigo Wolf,
- Lucas Farinazzo Marques,
- Lauana Fogaça de Almeida,
- Lucas Cardoso Lázari,
- Leonardo Nazário de Moraes,
- Luiz Henrique Cardoso,
- Camila Cristina de Oliveira Alves,
- Rafael Takahiro Nakajima,
- Amanda Piveta Schnepper,
- Marjorie de Assis Golim,
- Thais Regiani Cataldi,
- Jeroen G. Nijland,
- Camila Moreira Pinto,
- Matheus Naia Fioretto,
- Rodrigo Oliveira Almeida,
- Arnold J. M. Driessen,
- Rafael Plana Simōes,
- Mônica Veneziano Labate,
- Rejane Maria Tommasini Grotto,
- Carlos Alberto Labate,
- Ary Fernandes Junior,
- Luis Antonio Justulin,
- Rafael Luiz Buogo Coan,
- Érica Ramos,
- Fabiana Barcelos Furtado,
- Cesar Martins,
- Guilherme Targino Valente
Affiliations
- Ivan Rodrigo Wolf
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Lucas Farinazzo Marques
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Lauana Fogaça de Almeida
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Lucas Cardoso Lázari
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Leonardo Nazário de Moraes
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Luiz Henrique Cardoso
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Camila Cristina de Oliveira Alves
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Rafael Takahiro Nakajima
- Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Amanda Piveta Schnepper
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Marjorie de Assis Golim
- Laboratory of Applied Biotechnology, Clinical Hospital of the Medical School, São Paulo State University (UNESP), Botucatu 18618-970, Brazil
- Thais Regiani Cataldi
- Laboratório Max Feffer de Genética de Plantas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP), Piracicaba 13418-900, Brazil
- Jeroen G. Nijland
- Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands
- Camila Moreira Pinto
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Matheus Naia Fioretto
- Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Rodrigo Oliveira Almeida
- Instituto Federal de Educação, Ciência e Tecnologia do Sudeste de Minas Gerais–Campus Muriaé, Muriaé 36884-036, Brazil
- Arnold J. M. Driessen
- Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands
- Rafael Plana Simōes
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Mônica Veneziano Labate
- Laboratório Max Feffer de Genética de Plantas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP), Piracicaba 13418-900, Brazil
- Rejane Maria Tommasini Grotto
- Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, Brazil
- Carlos Alberto Labate
- Laboratório Max Feffer de Genética de Plantas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP), Piracicaba 13418-900, Brazil
- Ary Fernandes Junior
- Laboratory of Bacteriology, Department of Chemical and Biological Sciences, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Luis Antonio Justulin
- Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Rafael Luiz Buogo Coan
- Department of Biophysics and Pharmacology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Érica Ramos
- Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Fabiana Barcelos Furtado
- Laboratory of Applied Biotechnology, Clinical Hospital of the Medical School, São Paulo State University (UNESP), Botucatu 18618-970, Brazil
- Cesar Martins
- Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, Brazil
- Guilherme Targino Valente
- Max Planck Institute for Heart and Lung Research, 61231 Bad Nauheim, Germany
- DOI
- https://doi.org/10.3390/ijms24065646
- Journal volume & issue
-
Vol. 24,
no. 6
p. 5646
Abstract
Ethanol (EtOH) alters many cellular processes in yeast. An integrated view of different EtOH-tolerant phenotypes and their long noncoding RNAs (lncRNAs) is not yet available. Here, large-scale data integration showed the core EtOH-responsive pathways, lncRNAs, and triggers of higher (HT) and lower (LT) EtOH-tolerant phenotypes. LncRNAs act in a strain-specific manner in the EtOH stress response. Network and omics analyses revealed that cells prepare for stress relief by favoring activation of life-essential systems. Therefore, longevity, peroxisomal, energy, lipid, and RNA/protein metabolisms are the core processes that drive EtOH tolerance. By integrating omics, network analysis, and several other experiments, we showed how the HT and LT phenotypes may arise: (1) the divergence occurs after cell signaling reaches the longevity and peroxisomal pathways, with CTA1 and ROS playing key roles; (2) signals reaching essential ribosomal and RNA pathways via SUI2 enhance the divergence; (3) specific lipid metabolism pathways also act on phenotype-specific profiles; (4) HTs take greater advantage of degradation and membraneless structures to cope with EtOH stress; and (5) our EtOH stress-buffering model suggests that diauxic shift drives EtOH buffering through an energy burst, mainly in HTs. Finally, critical genes, pathways, and the first models including lncRNAs to describe nuances of EtOH tolerance are reported here.
Keywords