Abstract

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.

Original languageEnglish
Article number2510
JournalFrontiers in Microbiology
Volume10
DOIs
Publication statusPublished - 1 Nov 2019

Fingerprint

Mannitol
Fermentation
Yeasts
Glucose
Fructose
Oxidation-Reduction
Carbon
Horizontal Gene Transfer
Genomics
Glycerol
Molecular Biology
Ethanol
History
Mutation
Temperature

Keywords

  • alcoholic fermentation
  • fructophily
  • mannitol metabolism
  • Starmerella
  • yeast metabolism

Cite this

@article{4da1a1ff57b44ebda6a83c89e8e0341c,
title = "A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation",
abstract = "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.",
keywords = "alcoholic fermentation, fructophily, mannitol metabolism, Starmerella, yeast metabolism",
author = "Carla Gon{\cc}alves and Carolina Ferreira and Gon{\cc}alves, {Lu{\'i}s G.} and Turner, {David L.} and Leandro, {Maria Jos{\'e}} and Madalena Salema-Oom and Helena Santos and Paula Gon{\cc}alves",
note = "info:eu-repo/grantAgreement/FCT/SFRH/SFRH{\%}2FBD{\%}2F89489{\%}2F2012/PT# UID/Multi/04378/2019. FructYEAST - LISBOA-01-0145-FEDER-029529/PTDC/BIAMIC/29529/2017. LISBOA-01-0145-FEDER007660. AAC 01/SAICT/2016. SFRH/BPD/111100/2015. SFRH/BPD/102803/2014.",
year = "2019",
month = "11",
day = "1",
doi = "10.3389/fmicb.2019.02510",
language = "English",
volume = "10",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Research Foundation",

}

TY - JOUR

T1 - A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation

AU - Gonçalves, Carla

AU - Ferreira, Carolina

AU - Gonçalves, Luís G.

AU - Turner, David L.

AU - Leandro, Maria José

AU - Salema-Oom, Madalena

AU - Santos, Helena

AU - Gonçalves, Paula

N1 - info:eu-repo/grantAgreement/FCT/SFRH/SFRH%2FBD%2F89489%2F2012/PT# UID/Multi/04378/2019. FructYEAST - LISBOA-01-0145-FEDER-029529/PTDC/BIAMIC/29529/2017. LISBOA-01-0145-FEDER007660. AAC 01/SAICT/2016. SFRH/BPD/111100/2015. SFRH/BPD/102803/2014.

PY - 2019/11/1

Y1 - 2019/11/1

N2 - 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.

AB - 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.

KW - alcoholic fermentation

KW - fructophily

KW - mannitol metabolism

KW - Starmerella

KW - yeast metabolism

UR - http://www.scopus.com/inward/record.url?scp=85075257813&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2019.02510

DO - 10.3389/fmicb.2019.02510

M3 - Article

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 2510

ER -