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,...
Gespeichert in:
Veröffentlicht in: | Molecular ecology 2017-04, Vol.26 (7), p.2150-2166 |
---|---|
Hauptverfasser: | , , , , , , , , , |
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 & Sons Ltd</rights><rights>2017 John Wiley & Sons Ltd.</rights><rights>Copyright © 2017 John Wiley & 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 |