A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation

Detalhes bibliográficos
Autor(a) principal: Gonçalves, Carla
Data de Publicação: 2019
Outros Autores: Ferreira, Carolina, Gonçalves, Luís G., Turner, David L., Leandro, Maria José, Salema-Oom, Madalena, Santos, Helena, Gonçalves, Paula
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.26/30511
Resumo: This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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spelling A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentationAlcoholic fermentationYeast metabolismMannitol metabolismStarmerellaFructophilyThis is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.The yeasts belonging to the Wickerhamiella and Starmerella genera (W/S clade) share a distinctive evolutionary history marked by loss and subsequent reinstatement of alcoholic fermentation mediated by horizontal gene transfer events. Species in this clade also share unusual features of metabolism, namely the preference for fructose over glucose as carbon source, a rare trait known as fructophily. Here we show that fructose may be the preferred sugar in W/S-clade species because, unlike glucose, it can be converted directly to mannitol in a reaction with impact on redox balance. According to our results, mannitol is excreted to the growth medium in appreciable amounts along with other fermentation products such as glycerol and ethanol but unlike the latter metabolites mannitol production increases with temperature. We used comparative genomics to find genes involved in mannitol metabolism and established the mannitol biosynthesis pathway in W/S-clade species Starmerella bombicola using molecular genetics tools. Surprisingly, mannitol production seems to be so important that St. bombicola (and other W/S-clade species) deploys a novel pathway to mediate the conversion of glucose to fructose, thereby allowing cells to produce mannitol even when glucose is the sole carbon source. Using targeted mutations and 13C-labeled glucose followed by NMR analysis of end-products, we showed that the novel mannitol biosynthesis pathway involves fructose-6-phosphate as an intermediate, implying a key role for a yet unknown fructose-6-P phosphatase. We hypothesize that mannitol production contributed to mitigate the negative effects on redox balance of the ancient loss of alcoholic fermentation in the W/S clade. Presently, mannitol also seems to play a role in stress protection.Frontiers MediaRepositório ComumGonçalves, CarlaFerreira, CarolinaGonçalves, Luís G.Turner, David L.Leandro, Maria JoséSalema-Oom, MadalenaSantos, HelenaGonçalves, Paula2019-12-16T16:20:07Z2019-11-01T00:00:00Z2019-11-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.26/30511engGonçalves C, Ferreira C, Gonçalves LG, Turner DL, Leandro MJ, Salema-Oom M, Santos H and Gonçalves P (2019) A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation. Front. Microbiol. 10:2510. doi: 10.3389/fmicb.2019.025101664-302X10.3389/fmicb.2019.02510info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2022-10-06T14:53:56Zoai:comum.rcaap.pt:10400.26/30511Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T15:09:41.892020Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
title A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
spellingShingle A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
Gonçalves, Carla
Alcoholic fermentation
Yeast metabolism
Mannitol metabolism
Starmerella
Fructophily
title_short A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
title_full A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
title_fullStr A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
title_full_unstemmed A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
title_sort A new pathway for Mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation
author Gonçalves, Carla
author_facet Gonçalves, Carla
Ferreira, Carolina
Gonçalves, Luís G.
Turner, David L.
Leandro, Maria José
Salema-Oom, Madalena
Santos, Helena
Gonçalves, Paula
author_role author
author2 Ferreira, Carolina
Gonçalves, Luís G.
Turner, David L.
Leandro, Maria José
Salema-Oom, Madalena
Santos, Helena
Gonçalves, Paula
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Repositório Comum
dc.contributor.author.fl_str_mv Gonçalves, Carla
Ferreira, Carolina
Gonçalves, Luís G.
Turner, David L.
Leandro, Maria José
Salema-Oom, Madalena
Santos, Helena
Gonçalves, Paula
dc.subject.por.fl_str_mv Alcoholic fermentation
Yeast metabolism
Mannitol metabolism
Starmerella
Fructophily
topic Alcoholic fermentation
Yeast metabolism
Mannitol metabolism
Starmerella
Fructophily
description This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
publishDate 2019
dc.date.none.fl_str_mv 2019-12-16T16:20:07Z
2019-11-01T00:00:00Z
2019-11-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.26/30511
url http://hdl.handle.net/10400.26/30511
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Gonçalves C, Ferreira C, Gonçalves LG, Turner DL, Leandro MJ, Salema-Oom M, Santos H and Gonçalves P (2019) A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation. Front. Microbiol. 10:2510. doi: 10.3389/fmicb.2019.02510
1664-302X
10.3389/fmicb.2019.02510
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron_str RCAAP
institution RCAAP
reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
repository.mail.fl_str_mv
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