A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation
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, n...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.02510/full |
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| author | Carla Gonçalves Carolina Ferreira Luís G. Gonçalves David L. Turner Maria José Leandro Madalena Salema-Oom Madalena Salema-Oom Helena Santos Paula Gonçalves |
| author_facet | Carla Gonçalves Carolina Ferreira Luís G. Gonçalves David L. Turner Maria José Leandro Madalena Salema-Oom Madalena Salema-Oom Helena Santos Paula Gonçalves |
| author_sort | Carla Gonçalves |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-13T14:35:13Z |
| format | Article |
| id | doaj.art-737a14a870334e1283fb087ed7116698 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-13T14:35:13Z |
| publishDate | 2019-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-737a14a870334e1283fb087ed71166982022-12-21T23:41:45ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02510492827A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic FermentationCarla Gonçalves0Carolina Ferreira1Luís G. Gonçalves2David L. Turner3Maria José Leandro4Madalena Salema-Oom5Madalena Salema-Oom6Helena Santos7Paula Gonçalves8UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, PortugalUCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, PortugalInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalUCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, PortugalCentro de Investigação Interdisciplinar Egas Moniz (CiiEM), Instituto Universitário Egas Moniz, Caparica, PortugalInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalUCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, PortugalThe 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.02510/fullalcoholic fermentationyeast metabolismmannitol metabolismStarmerellafructophily |
| spellingShingle | Carla Gonçalves Carolina Ferreira Luís G. Gonçalves David L. Turner Maria José Leandro Madalena Salema-Oom Madalena Salema-Oom Helena Santos Paula Gonçalves A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation Frontiers in Microbiology alcoholic fermentation yeast metabolism mannitol metabolism Starmerella fructophily |
| title | 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_short | A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation |
| title_sort | new pathway for mannitol metabolism in yeasts suggests a link to the evolution of alcoholic fermentation |
| topic | alcoholic fermentation yeast metabolism mannitol metabolism Starmerella fructophily |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.02510/full |
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