Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts

The molecular and evolutionary processes underlying fungal domestication remain largely unknown despite the importance of fungi to bioindustry and for comparative adaptation genomics in eukaryotes. Wine fermentation and biological ageing are performed by strains of S. cerevisiae with, respectively,...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Molecular ecology 2017-04, Vol.26 (7), p.2150-2166
Hauptverfasser: Coi, A. L., Bigey, F., Mallet, S., Marsit, S., Zara, G., Gladieux, P., Galeote, V., Budroni, M., Dequin, S., Legras, J. L.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 2166
container_issue 7
container_start_page 2150
container_title Molecular ecology
container_volume 26
creator Coi, A. L.
Bigey, F.
Mallet, S.
Marsit, S.
Zara, G.
Gladieux, P.
Galeote, V.
Budroni, M.
Dequin, S.
Legras, J. L.
description The molecular and evolutionary processes underlying fungal domestication remain largely unknown despite the importance of fungi to bioindustry and for comparative adaptation genomics in eukaryotes. Wine fermentation and biological ageing are performed by strains of S. cerevisiae with, respectively, pelagic fermentative growth on glucose and biofilm aerobic growth utilizing ethanol. Here, we use environmental samples of wine and flor yeasts to investigate the genomic basis of yeast adaptation to contrasted anthropogenic environments. Phylogenetic inference and population structure analysis based on single nucleotide polymorphisms revealed a group of flor yeasts separated from wine yeasts. A combination of methods revealed several highly differentiated regions between wine and flor yeasts, and analyses using codon‐substitution models for detecting molecular adaptation identified sites under positive selection in the high‐affinity transporter gene ZRT1. The cross‐population composite likelihood ratio revealed selective sweeps at three regions, including in the hexose transporter gene HXT7, the yapsin gene YPS6 and the membrane protein coding gene MTS27. Our analyses also revealed that the biological ageing environment has led to the accumulation of numerous mutations in proteins from several networks, including Flo11 regulation and divalent metal transport. Together, our findings suggest that the tuning of FLO11 expression and zinc transport networks are a distinctive feature of the genetic changes underlying the domestication of flor yeasts. Our study highlights the multiplicity of genomic changes underlying yeast adaptation to man‐made habitats and reveals that flor/wine yeast lineage can serve as a useful model for studying the genomics of adaptive divergence.
doi_str_mv 10.1111/mec.14053
format Article
fullrecord <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_01608516v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1891881564</sourcerecordid><originalsourceid>FETCH-LOGICAL-c5253-9c6dba55dbfba14015ae72c9848bcb3e78b1ac01662d4adf0ca2bba9484dda613</originalsourceid><addsrcrecordid>eNqNkc9q3DAQxkVpaLZpD32BIuilPTiRZEsrHcOSP4UNvbTQmxjJ8lbBlraSnbC3PkKeMU8SuZvuoVDoXAZmfvMxHx9C7yg5paXOBmdPaUN4_QItaC14xVTz_SVaECVYRYmsj9HrnG8JoTXj_BU6ZpIqJqhaoO7KhTh4i7PfBBin5DKOHYYWtiOMPgY8Rnzvg8PGxz5uvIUew8b5sME2htbPTMY-zPvO98Pjr4cupmHed31MeOcgj_kNOuqgz-7tcz9B3y4vvq6uq_WXq8-r83VlOeN1paxoDXDems5AcUQ5uCWzSjbSWFO7pTQULKFCsLaBtiMWmDGgGtm0LQhan6BPe90f0Ott8gOknY7g9fX5Ws-zckskp-JuZj_u2W2KPyeXRz34bF3fQ3BxyppKRaWkXDT_gQpZK6GkLOiHv9DbOKVQTBdKLikhrDg9_GlTzDm57vAsJXrOVJdM9e9MC_v-WXEyg2sP5J8QC3C2B-5973b_VtI3F6u95BN0mqvr</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1887100225</pqid></control><display><type>article</type><title>Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><creator>Coi, A. L. ; Bigey, F. ; Mallet, S. ; Marsit, S. ; Zara, G. ; Gladieux, P. ; Galeote, V. ; Budroni, M. ; Dequin, S. ; Legras, J. L.</creator><creatorcontrib>Coi, A. L. ; Bigey, F. ; Mallet, S. ; Marsit, S. ; Zara, G. ; Gladieux, P. ; Galeote, V. ; Budroni, M. ; Dequin, S. ; Legras, J. L.</creatorcontrib><description>The molecular and evolutionary processes underlying fungal domestication remain largely unknown despite the importance of fungi to bioindustry and for comparative adaptation genomics in eukaryotes. Wine fermentation and biological ageing are performed by strains of S. cerevisiae with, respectively, pelagic fermentative growth on glucose and biofilm aerobic growth utilizing ethanol. Here, we use environmental samples of wine and flor yeasts to investigate the genomic basis of yeast adaptation to contrasted anthropogenic environments. Phylogenetic inference and population structure analysis based on single nucleotide polymorphisms revealed a group of flor yeasts separated from wine yeasts. A combination of methods revealed several highly differentiated regions between wine and flor yeasts, and analyses using codon‐substitution models for detecting molecular adaptation identified sites under positive selection in the high‐affinity transporter gene ZRT1. The cross‐population composite likelihood ratio revealed selective sweeps at three regions, including in the hexose transporter gene HXT7, the yapsin gene YPS6 and the membrane protein coding gene MTS27. Our analyses also revealed that the biological ageing environment has led to the accumulation of numerous mutations in proteins from several networks, including Flo11 regulation and divalent metal transport. Together, our findings suggest that the tuning of FLO11 expression and zinc transport networks are a distinctive feature of the genetic changes underlying the domestication of flor yeasts. Our study highlights the multiplicity of genomic changes underlying yeast adaptation to man‐made habitats and reveals that flor/wine yeast lineage can serve as a useful model for studying the genomics of adaptive divergence.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.14053</identifier><identifier>PMID: 28192619</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>adaptation ; Adaptation, Physiological - genetics ; Agricultural sciences ; biofilm ; Biofilms ; biological ageing ; Biotechnology ; domestication ; Fermentation ; FLO11 ; flor yeast ; Genetics, Population ; genome ; Genome, Fungal ; Life Sciences ; Phenotype ; Phylogeny ; Polymorphism, Single Nucleotide ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Selection, Genetic ; Vitaceae ; Wine - microbiology ; ZRT1</subject><ispartof>Molecular ecology, 2017-04, Vol.26 (7), p.2150-2166</ispartof><rights>2017 John Wiley &amp; Sons Ltd</rights><rights>2017 John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2017 John Wiley &amp; Sons Ltd</rights><rights>Attribution - ShareAlike</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5253-9c6dba55dbfba14015ae72c9848bcb3e78b1ac01662d4adf0ca2bba9484dda613</citedby><cites>FETCH-LOGICAL-c5253-9c6dba55dbfba14015ae72c9848bcb3e78b1ac01662d4adf0ca2bba9484dda613</cites><orcidid>0000-0002-4006-4389 ; 0000-0002-6240-3038 ; 0000-0003-1929-1576 ; 0000-0001-8929-8672 ; 0000-0002-9114-2324</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.14053$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.14053$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28192619$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01608516$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Coi, A. L.</creatorcontrib><creatorcontrib>Bigey, F.</creatorcontrib><creatorcontrib>Mallet, S.</creatorcontrib><creatorcontrib>Marsit, S.</creatorcontrib><creatorcontrib>Zara, G.</creatorcontrib><creatorcontrib>Gladieux, P.</creatorcontrib><creatorcontrib>Galeote, V.</creatorcontrib><creatorcontrib>Budroni, M.</creatorcontrib><creatorcontrib>Dequin, S.</creatorcontrib><creatorcontrib>Legras, J. L.</creatorcontrib><title>Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>The molecular and evolutionary processes underlying fungal domestication remain largely unknown despite the importance of fungi to bioindustry and for comparative adaptation genomics in eukaryotes. Wine fermentation and biological ageing are performed by strains of S. cerevisiae with, respectively, pelagic fermentative growth on glucose and biofilm aerobic growth utilizing ethanol. Here, we use environmental samples of wine and flor yeasts to investigate the genomic basis of yeast adaptation to contrasted anthropogenic environments. Phylogenetic inference and population structure analysis based on single nucleotide polymorphisms revealed a group of flor yeasts separated from wine yeasts. A combination of methods revealed several highly differentiated regions between wine and flor yeasts, and analyses using codon‐substitution models for detecting molecular adaptation identified sites under positive selection in the high‐affinity transporter gene ZRT1. The cross‐population composite likelihood ratio revealed selective sweeps at three regions, including in the hexose transporter gene HXT7, the yapsin gene YPS6 and the membrane protein coding gene MTS27. Our analyses also revealed that the biological ageing environment has led to the accumulation of numerous mutations in proteins from several networks, including Flo11 regulation and divalent metal transport. Together, our findings suggest that the tuning of FLO11 expression and zinc transport networks are a distinctive feature of the genetic changes underlying the domestication of flor yeasts. Our study highlights the multiplicity of genomic changes underlying yeast adaptation to man‐made habitats and reveals that flor/wine yeast lineage can serve as a useful model for studying the genomics of adaptive divergence.</description><subject>adaptation</subject><subject>Adaptation, Physiological - genetics</subject><subject>Agricultural sciences</subject><subject>biofilm</subject><subject>Biofilms</subject><subject>biological ageing</subject><subject>Biotechnology</subject><subject>domestication</subject><subject>Fermentation</subject><subject>FLO11</subject><subject>flor yeast</subject><subject>Genetics, Population</subject><subject>genome</subject><subject>Genome, Fungal</subject><subject>Life Sciences</subject><subject>Phenotype</subject><subject>Phylogeny</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Selection, Genetic</subject><subject>Vitaceae</subject><subject>Wine - microbiology</subject><subject>ZRT1</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc9q3DAQxkVpaLZpD32BIuilPTiRZEsrHcOSP4UNvbTQmxjJ8lbBlraSnbC3PkKeMU8SuZvuoVDoXAZmfvMxHx9C7yg5paXOBmdPaUN4_QItaC14xVTz_SVaECVYRYmsj9HrnG8JoTXj_BU6ZpIqJqhaoO7KhTh4i7PfBBin5DKOHYYWtiOMPgY8Rnzvg8PGxz5uvIUew8b5sME2htbPTMY-zPvO98Pjr4cupmHed31MeOcgj_kNOuqgz-7tcz9B3y4vvq6uq_WXq8-r83VlOeN1paxoDXDems5AcUQ5uCWzSjbSWFO7pTQULKFCsLaBtiMWmDGgGtm0LQhan6BPe90f0Ott8gOknY7g9fX5Ws-zckskp-JuZj_u2W2KPyeXRz34bF3fQ3BxyppKRaWkXDT_gQpZK6GkLOiHv9DbOKVQTBdKLikhrDg9_GlTzDm57vAsJXrOVJdM9e9MC_v-WXEyg2sP5J8QC3C2B-5973b_VtI3F6u95BN0mqvr</recordid><startdate>201704</startdate><enddate>201704</enddate><creator>Coi, A. L.</creator><creator>Bigey, F.</creator><creator>Mallet, S.</creator><creator>Marsit, S.</creator><creator>Zara, G.</creator><creator>Gladieux, P.</creator><creator>Galeote, V.</creator><creator>Budroni, M.</creator><creator>Dequin, S.</creator><creator>Legras, J. L.</creator><general>Blackwell Publishing Ltd</general><general>Wiley</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-4006-4389</orcidid><orcidid>https://orcid.org/0000-0002-6240-3038</orcidid><orcidid>https://orcid.org/0000-0003-1929-1576</orcidid><orcidid>https://orcid.org/0000-0001-8929-8672</orcidid><orcidid>https://orcid.org/0000-0002-9114-2324</orcidid></search><sort><creationdate>201704</creationdate><title>Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts</title><author>Coi, A. L. ; Bigey, F. ; Mallet, S. ; Marsit, S. ; Zara, G. ; Gladieux, P. ; Galeote, V. ; Budroni, M. ; Dequin, S. ; Legras, J. L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5253-9c6dba55dbfba14015ae72c9848bcb3e78b1ac01662d4adf0ca2bba9484dda613</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>adaptation</topic><topic>Adaptation, Physiological - genetics</topic><topic>Agricultural sciences</topic><topic>biofilm</topic><topic>Biofilms</topic><topic>biological ageing</topic><topic>Biotechnology</topic><topic>domestication</topic><topic>Fermentation</topic><topic>FLO11</topic><topic>flor yeast</topic><topic>Genetics, Population</topic><topic>genome</topic><topic>Genome, Fungal</topic><topic>Life Sciences</topic><topic>Phenotype</topic><topic>Phylogeny</topic><topic>Polymorphism, Single Nucleotide</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Selection, Genetic</topic><topic>Vitaceae</topic><topic>Wine - microbiology</topic><topic>ZRT1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Coi, A. L.</creatorcontrib><creatorcontrib>Bigey, F.</creatorcontrib><creatorcontrib>Mallet, S.</creatorcontrib><creatorcontrib>Marsit, S.</creatorcontrib><creatorcontrib>Zara, G.</creatorcontrib><creatorcontrib>Gladieux, P.</creatorcontrib><creatorcontrib>Galeote, V.</creatorcontrib><creatorcontrib>Budroni, M.</creatorcontrib><creatorcontrib>Dequin, S.</creatorcontrib><creatorcontrib>Legras, J. L.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Coi, A. L.</au><au>Bigey, F.</au><au>Mallet, S.</au><au>Marsit, S.</au><au>Zara, G.</au><au>Gladieux, P.</au><au>Galeote, V.</au><au>Budroni, M.</au><au>Dequin, S.</au><au>Legras, J. L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2017-04</date><risdate>2017</risdate><volume>26</volume><issue>7</issue><spage>2150</spage><epage>2166</epage><pages>2150-2166</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>The molecular and evolutionary processes underlying fungal domestication remain largely unknown despite the importance of fungi to bioindustry and for comparative adaptation genomics in eukaryotes. Wine fermentation and biological ageing are performed by strains of S. cerevisiae with, respectively, pelagic fermentative growth on glucose and biofilm aerobic growth utilizing ethanol. Here, we use environmental samples of wine and flor yeasts to investigate the genomic basis of yeast adaptation to contrasted anthropogenic environments. Phylogenetic inference and population structure analysis based on single nucleotide polymorphisms revealed a group of flor yeasts separated from wine yeasts. A combination of methods revealed several highly differentiated regions between wine and flor yeasts, and analyses using codon‐substitution models for detecting molecular adaptation identified sites under positive selection in the high‐affinity transporter gene ZRT1. The cross‐population composite likelihood ratio revealed selective sweeps at three regions, including in the hexose transporter gene HXT7, the yapsin gene YPS6 and the membrane protein coding gene MTS27. Our analyses also revealed that the biological ageing environment has led to the accumulation of numerous mutations in proteins from several networks, including Flo11 regulation and divalent metal transport. Together, our findings suggest that the tuning of FLO11 expression and zinc transport networks are a distinctive feature of the genetic changes underlying the domestication of flor yeasts. Our study highlights the multiplicity of genomic changes underlying yeast adaptation to man‐made habitats and reveals that flor/wine yeast lineage can serve as a useful model for studying the genomics of adaptive divergence.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>28192619</pmid><doi>10.1111/mec.14053</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-4006-4389</orcidid><orcidid>https://orcid.org/0000-0002-6240-3038</orcidid><orcidid>https://orcid.org/0000-0003-1929-1576</orcidid><orcidid>https://orcid.org/0000-0001-8929-8672</orcidid><orcidid>https://orcid.org/0000-0002-9114-2324</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0962-1083
ispartof Molecular ecology, 2017-04, Vol.26 (7), p.2150-2166
issn 0962-1083
1365-294X
language eng
recordid cdi_hal_primary_oai_HAL_hal_01608516v1
source MEDLINE; Wiley Online Library Journals Frontfile Complete
subjects adaptation
Adaptation, Physiological - genetics
Agricultural sciences
biofilm
Biofilms
biological ageing
Biotechnology
domestication
Fermentation
FLO11
flor yeast
Genetics, Population
genome
Genome, Fungal
Life Sciences
Phenotype
Phylogeny
Polymorphism, Single Nucleotide
Saccharomyces cerevisiae
Saccharomyces cerevisiae - genetics
Selection, Genetic
Vitaceae
Wine - microbiology
ZRT1
title Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-24T12%3A24%3A07IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Genomic%20signatures%20of%20adaptation%20to%20wine%20biological%20ageing%20conditions%20in%20biofilm%E2%80%90forming%20flor%20yeasts&rft.jtitle=Molecular%20ecology&rft.au=Coi,%20A.%20L.&rft.date=2017-04&rft.volume=26&rft.issue=7&rft.spage=2150&rft.epage=2166&rft.pages=2150-2166&rft.issn=0962-1083&rft.eissn=1365-294X&rft_id=info:doi/10.1111/mec.14053&rft_dat=%3Cproquest_hal_p%3E1891881564%3C/proquest_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1887100225&rft_id=info:pmid/28192619&rfr_iscdi=true