Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i>
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 (...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-03-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/24/6/5646 |
| _version_ | 1797611261153771520 |
|---|---|
| author | 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 |
| author_facet | 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 |
| author_sort | Ivan Rodrigo Wolf |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-11T06:25:19Z |
| format | Article |
| id | doaj.art-b3041eb4384446098a818c7e3845bb7f |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-11T06:25:19Z |
| publishDate | 2023-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-b3041eb4384446098a818c7e3845bb7f2023-11-17T11:36:58ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-03-01246564610.3390/ijms24065646Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i>Ivan Rodrigo Wolf0Lucas Farinazzo Marques1Lauana Fogaça de Almeida2Lucas Cardoso Lázari3Leonardo Nazário de Moraes4Luiz Henrique Cardoso5Camila Cristina de Oliveira Alves6Rafael Takahiro Nakajima7Amanda Piveta Schnepper8Marjorie de Assis Golim9Thais Regiani Cataldi10Jeroen G. Nijland11Camila Moreira Pinto12Matheus Naia Fioretto13Rodrigo Oliveira Almeida14Arnold J. M. Driessen15Rafael Plana Simōes16Mônica Veneziano Labate17Rejane Maria Tommasini Grotto18Carlos Alberto Labate19Ary Fernandes Junior20Luis Antonio Justulin21Rafael Luiz Buogo Coan22Érica Ramos23Fabiana Barcelos Furtado24Cesar Martins25Guilherme Targino Valente26Department of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilLaboratory of Applied Biotechnology, Clinical Hospital of the Medical School, São Paulo State University (UNESP), Botucatu 18618-970, BrazilLaboratório Max Feffer de Genética de Plantas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP), Piracicaba 13418-900, BrazilMolecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The NetherlandsDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilDepartment of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilInstituto Federal de Educação, Ciência e Tecnologia do Sudeste de Minas Gerais–Campus Muriaé, Muriaé 36884-036, BrazilMolecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The NetherlandsDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilLaboratório Max Feffer de Genética de Plantas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP), Piracicaba 13418-900, BrazilDepartment of Bioprocess and Biotechnology, School of Agriculture, São Paulo State University (UNESP), Botucatu 18610-034, BrazilLaboratório Max Feffer de Genética de Plantas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP), Piracicaba 13418-900, BrazilLaboratory of Bacteriology, Department of Chemical and Biological Sciences, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilDepartment of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilDepartment of Biophysics and Pharmacology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilDepartment of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilLaboratory of Applied Biotechnology, Clinical Hospital of the Medical School, São Paulo State University (UNESP), Botucatu 18618-970, BrazilDepartment of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu 18618-689, BrazilMax Planck Institute for Heart and Lung Research, 61231 Bad Nauheim, GermanyEthanol (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.https://www.mdpi.com/1422-0067/24/6/5646omicsdata integrationsystems biologylncRNAslncRNA–protein interactionsmembraneless organelles |
| spellingShingle | 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 Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i> International Journal of Molecular Sciences omics data integration systems biology lncRNAs lncRNA–protein interactions membraneless organelles |
| title | Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i> |
| title_full | Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i> |
| title_fullStr | Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i> |
| title_full_unstemmed | Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i> |
| title_short | Integrative Analysis of the Ethanol Tolerance of <i>Saccharomyces cerevisiae</i> |
| title_sort | integrative analysis of the ethanol tolerance of i saccharomyces cerevisiae i |
| topic | omics data integration systems biology lncRNAs lncRNA–protein interactions membraneless organelles |
| url | https://www.mdpi.com/1422-0067/24/6/5646 |
| work_keys_str_mv | AT ivanrodrigowolf integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT lucasfarinazzomarques integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT lauanafogacadealmeida integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT lucascardosolazari integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT leonardonazariodemoraes integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT luizhenriquecardoso integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT camilacristinadeoliveiraalves integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT rafaeltakahironakajima integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT amandapivetaschnepper integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT marjoriedeassisgolim integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT thaisregianicataldi integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT jeroengnijland integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT camilamoreirapinto integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT matheusnaiafioretto integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT rodrigooliveiraalmeida integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT arnoldjmdriessen integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT rafaelplanasimoes integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT monicavenezianolabate integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT rejanemariatommasinigrotto integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT carlosalbertolabate integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT aryfernandesjunior integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT luisantoniojustulin integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT rafaelluizbuogocoan integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT ericaramos integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT fabianabarcelosfurtado integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT cesarmartins integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei AT guilhermetarginovalente integrativeanalysisoftheethanoltoleranceofisaccharomycescerevisiaei |