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Evolutionary engineering and molecular characterization of a caffeine-resistant Saccharomyces cerevisiae strain.

Identifieur interne : 000346 ( Main/Exploration ); précédent : 000345; suivant : 000347

Evolutionary engineering and molecular characterization of a caffeine-resistant Saccharomyces cerevisiae strain.

Auteurs : Yusuf Sürmeli [Turquie] ; Can Holyavkin [Turquie] ; Alican Topalo Lu [Turquie] ; Mevlüt Arslan [Turquie] ; Halil Brahim K Sakesen [Turquie] ; Zeynep Petek Çakar [Turquie]

Source :

RBID : pubmed:31728740

Descripteurs français

English descriptors

Abstract

Caffeine is a naturally occurring alkaloid, where its major consumption occurs with beverages such as coffee, soft drinks and tea. Despite a variety of reports on the effects of caffeine on diverse organisms including yeast, the complex molecular basis of caffeine resistance and response has yet to be understood. In this study, a caffeine-hyperresistant and genetically stable Saccharomyces cerevisiae mutant was obtained for the first time by evolutionary engineering, using batch selection in the presence of gradually increased caffeine stress levels and without any mutagenesis of the initial population prior to selection. The selected mutant could resist up to 50 mM caffeine, a level, to our knowledge, that has not been reported for S. cerevisiae so far. The mutant was also resistant to the cell wall-damaging agent lyticase, and it showed cross-resistance against various compounds such as rapamycin, antimycin, coniferyl aldehyde and cycloheximide. Comparative transcriptomic analysis results revealed that the genes involved in the energy conservation and production pathways, and pleiotropic drug resistance were overexpressed. Whole genome re-sequencing identified single nucleotide polymorphisms in only three genes of the caffeine-hyperresistant mutant; PDR1, PDR5 and RIM8, which may play a potential role in caffeine-hyperresistance.

DOI: 10.1007/s11274-019-2762-2
PubMed: 31728740


Affiliations:


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<div type="abstract" xml:lang="en">Caffeine is a naturally occurring alkaloid, where its major consumption occurs with beverages such as coffee, soft drinks and tea. Despite a variety of reports on the effects of caffeine on diverse organisms including yeast, the complex molecular basis of caffeine resistance and response has yet to be understood. In this study, a caffeine-hyperresistant and genetically stable Saccharomyces cerevisiae mutant was obtained for the first time by evolutionary engineering, using batch selection in the presence of gradually increased caffeine stress levels and without any mutagenesis of the initial population prior to selection. The selected mutant could resist up to 50 mM caffeine, a level, to our knowledge, that has not been reported for S. cerevisiae so far. The mutant was also resistant to the cell wall-damaging agent lyticase, and it showed cross-resistance against various compounds such as rapamycin, antimycin, coniferyl aldehyde and cycloheximide. Comparative transcriptomic analysis results revealed that the genes involved in the energy conservation and production pathways, and pleiotropic drug resistance were overexpressed. Whole genome re-sequencing identified single nucleotide polymorphisms in only three genes of the caffeine-hyperresistant mutant; PDR1, PDR5 and RIM8, which may play a potential role in caffeine-hyperresistance.</div>
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<Journal>
<ISSN IssnType="Electronic">1573-0972</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>35</Volume>
<Issue>12</Issue>
<PubDate>
<Year>2019</Year>
<Month>Nov</Month>
<Day>14</Day>
</PubDate>
</JournalIssue>
<Title>World journal of microbiology & biotechnology</Title>
<ISOAbbreviation>World J Microbiol Biotechnol</ISOAbbreviation>
</Journal>
<ArticleTitle>Evolutionary engineering and molecular characterization of a caffeine-resistant Saccharomyces cerevisiae strain.</ArticleTitle>
<Pagination>
<MedlinePgn>183</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1007/s11274-019-2762-2</ELocationID>
<Abstract>
<AbstractText>Caffeine is a naturally occurring alkaloid, where its major consumption occurs with beverages such as coffee, soft drinks and tea. Despite a variety of reports on the effects of caffeine on diverse organisms including yeast, the complex molecular basis of caffeine resistance and response has yet to be understood. In this study, a caffeine-hyperresistant and genetically stable Saccharomyces cerevisiae mutant was obtained for the first time by evolutionary engineering, using batch selection in the presence of gradually increased caffeine stress levels and without any mutagenesis of the initial population prior to selection. The selected mutant could resist up to 50 mM caffeine, a level, to our knowledge, that has not been reported for S. cerevisiae so far. The mutant was also resistant to the cell wall-damaging agent lyticase, and it showed cross-resistance against various compounds such as rapamycin, antimycin, coniferyl aldehyde and cycloheximide. Comparative transcriptomic analysis results revealed that the genes involved in the energy conservation and production pathways, and pleiotropic drug resistance were overexpressed. Whole genome re-sequencing identified single nucleotide polymorphisms in only three genes of the caffeine-hyperresistant mutant; PDR1, PDR5 and RIM8, which may play a potential role in caffeine-hyperresistance.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Sürmeli</LastName>
<ForeName>Yusuf</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology and Genetics, Faculty of Science & Letters, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (İTÜ-MOBGAM), Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Agricultural Biotechnology, Faculty of Agriculture, Namık Kemal University, 59030, Tekirdağ, Turkey.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Holyavkin</LastName>
<ForeName>Can</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology and Genetics, Faculty of Science & Letters, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (İTÜ-MOBGAM), Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Topaloğlu</LastName>
<ForeName>Alican</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology and Genetics, Faculty of Science & Letters, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (İTÜ-MOBGAM), Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Arslan</LastName>
<ForeName>Mevlüt</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology and Genetics, Faculty of Science & Letters, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (İTÜ-MOBGAM), Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Genetics, Faculty of Veterinary Medicine, Van Yüzüncü Yıl University, 65080, Van, Turkey.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kısakesen</LastName>
<ForeName>Halil İbrahim</ForeName>
<Initials></Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology and Genetics, Faculty of Science & Letters, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (İTÜ-MOBGAM), Istanbul Technical University, Maslak, 34469, Istanbul, Turkey.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Çakar</LastName>
<ForeName>Zeynep Petek</ForeName>
<Initials>ZP</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-2278-3670</Identifier>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology and Genetics, Faculty of Science & Letters, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey. cakarp@itu.edu.tr.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (İTÜ-MOBGAM), Istanbul Technical University, Maslak, 34469, Istanbul, Turkey. cakarp@itu.edu.tr.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
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</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>11</Month>
<Day>14</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>Germany</Country>
<MedlineTA>World J Microbiol Biotechnol</MedlineTA>
<NlmUniqueID>9012472</NlmUniqueID>
<ISSNLinking>0959-3993</ISSNLinking>
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<Chemical>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
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<Chemical>
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<RegistryNumber>06TPT01AD5</RegistryNumber>
<NameOfSubstance UI="C075384">coniferaldehyde</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>11118-72-2</RegistryNumber>
<NameOfSubstance UI="C032456">antimycin</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>3G6A5W338E</RegistryNumber>
<NameOfSubstance UI="D002110">Caffeine</NameOfSubstance>
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<Chemical>
<RegistryNumber>642-15-9</RegistryNumber>
<NameOfSubstance UI="D000968">Antimycin A</NameOfSubstance>
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<Chemical>
<RegistryNumber>7864XYD3JJ</RegistryNumber>
<NameOfSubstance UI="D000171">Acrolein</NameOfSubstance>
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<Chemical>
<RegistryNumber>98600C0908</RegistryNumber>
<NameOfSubstance UI="D003513">Cycloheximide</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>W36ZG6FT64</RegistryNumber>
<NameOfSubstance UI="D020123">Sirolimus</NameOfSubstance>
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<MeshHeading>
<DescriptorName UI="D018528" MajorTopicYN="N">ATP-Binding Cassette Transporters</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000171" MajorTopicYN="N">Acrolein</DescriptorName>
<QualifierName UI="Q000031" MajorTopicYN="N">analogs & derivatives</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000968" MajorTopicYN="N">Antimycin A</DescriptorName>
<QualifierName UI="Q000031" MajorTopicYN="N">analogs & derivatives</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
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<MeshHeading>
<DescriptorName UI="D002110" MajorTopicYN="N">Caffeine</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
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<DescriptorName UI="D018797" MajorTopicYN="N">Cell Cycle Proteins</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D004268" MajorTopicYN="N">DNA-Binding Proteins</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D025141" MajorTopicYN="N">Drug Resistance, Fungal</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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<MeshHeading>
<DescriptorName UI="D016296" MajorTopicYN="N">Mutagenesis</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D020641" MajorTopicYN="N">Polymorphism, Single Nucleotide</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D015202" MajorTopicYN="N">Protein Engineering</DescriptorName>
<QualifierName UI="Q000379" MajorTopicYN="Y">methods</QualifierName>
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<MeshHeading>
<DescriptorName UI="D012441" MajorTopicYN="N">Saccharomyces cerevisiae</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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<MeshHeading>
<DescriptorName UI="D029701" MajorTopicYN="N">Saccharomyces cerevisiae Proteins</DescriptorName>
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<DescriptorName UI="D013312" MajorTopicYN="N">Stress, Physiological</DescriptorName>
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<DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
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<DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName>
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<DescriptorName UI="D000073336" MajorTopicYN="N">Whole Genome Sequencing</DescriptorName>
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<Keyword MajorTopicYN="N">Adaptive laboratory evolution</Keyword>
<Keyword MajorTopicYN="N">Caffeine</Keyword>
<Keyword MajorTopicYN="N">Evolutionary engineering</Keyword>
<Keyword MajorTopicYN="N">Pleiotropic drug resistance (PDR)</Keyword>
<Keyword MajorTopicYN="N">Saccharomyces cerevisiae</Keyword>
<Keyword MajorTopicYN="N">Stress resistance</Keyword>
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