Adaptability of the Saccharomyces cerevisiae yeasts to wine fermentation conditions relies on their strong ability to consume nitrogen

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Abstract

Saccharomyces cerevisiae strains are genetically diverse, largely as a result of human efforts to develop strains specifically adapted to various fermentation processes. These adaptive pressures from various ecological niches have generated behavioral differences among these strains, particularly in terms of their nitrogen consumption capacities. In this work, we characterize this phenotype by the specific quantity of nitrogen consumed under oenological fermentation conditions using a new approach. Indeed, unlike previous studies, our experiments were conducted in an environment containing excess nitrogen, eliminating the nitrogen limitation/starvation factor that is generally observed in fermentation processes. Using these conditions, we evaluated differences in the nitrogen consumption capacities for a set of five strains from diverse origins. The strains presented extremely different phenotypes and variations in their capacities to take up nitrogen from a wine fermentation environment. These variations reflect the differences in the nitrogen uptake capacities between wine and non-wine strains. Finally, the strains differed in their ability to adapt to the nitrogen composition of the environment, leading to variations in the cellular stress states, fermentation performances and the activity of the nitrogen sensing signaling pathway. © 2018 Brice et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
LanguageEnglish
JournalPLoS One
Volume13
Issue number2
DOIs
Publication statusPublished - 2018

Fingerprint

Wine
Yeast
Fermentation
Saccharomyces cerevisiae
wines
Nitrogen
Yeasts
fermentation
yeasts
nitrogen
Phenotype
phenotype
Licensure
Starvation
Reproduction
starvation
niches
uptake mechanisms
Pressure

Keywords

  • nitrogen
  • Article
  • cell culture
  • cell stress
  • comparative study
  • controlled study
  • evolutionary adaptation
  • fermentation
  • fungal strain
  • gene library
  • nitrogen uptake
  • nonhuman
  • phenotype
  • RNA extraction
  • RNA sequence
  • Saccharomyces cerevisiae
  • Saccharomyces cerevisiae 59A
  • Saccharomyces cerevisiae A390D2
  • Saccharomyces cerevisiae DBVPG6044
  • Saccharomyces cerevisiae Y12
  • Saccharomyces cerevisiae YPS128
  • signal transduction
  • starvation
  • strain difference
  • transcriptomics
  • wine

Cite this

@article{9e1d16a3d0d84f1da65f0bc2f66ef011,
title = "Adaptability of the Saccharomyces cerevisiae yeasts to wine fermentation conditions relies on their strong ability to consume nitrogen",
abstract = "Saccharomyces cerevisiae strains are genetically diverse, largely as a result of human efforts to develop strains specifically adapted to various fermentation processes. These adaptive pressures from various ecological niches have generated behavioral differences among these strains, particularly in terms of their nitrogen consumption capacities. In this work, we characterize this phenotype by the specific quantity of nitrogen consumed under oenological fermentation conditions using a new approach. Indeed, unlike previous studies, our experiments were conducted in an environment containing excess nitrogen, eliminating the nitrogen limitation/starvation factor that is generally observed in fermentation processes. Using these conditions, we evaluated differences in the nitrogen consumption capacities for a set of five strains from diverse origins. The strains presented extremely different phenotypes and variations in their capacities to take up nitrogen from a wine fermentation environment. These variations reflect the differences in the nitrogen uptake capacities between wine and non-wine strains. Finally, the strains differed in their ability to adapt to the nitrogen composition of the environment, leading to variations in the cellular stress states, fermentation performances and the activity of the nitrogen sensing signaling pathway. {\circledC} 2018 Brice et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",
keywords = "nitrogen, Article, cell culture, cell stress, comparative study, controlled study, evolutionary adaptation, fermentation, fungal strain, gene library, nitrogen uptake, nonhuman, phenotype, RNA extraction, RNA sequence, Saccharomyces cerevisiae, Saccharomyces cerevisiae 59A, Saccharomyces cerevisiae A390D2, Saccharomyces cerevisiae DBVPG6044, Saccharomyces cerevisiae Y12, Saccharomyces cerevisiae YPS128, signal transduction, starvation, strain difference, transcriptomics, wine",
author = "C. Brice and S. Dequin and C. Camarasa and {Cubillos Riffo}, {Francisco A.} and {Cubillos Riffo}, {Francisco A.} and {Martinez Fernandez}, {Claudio A.} and {Martinez Fernandez}, {Claudio A.}",
note = "Export Date: 26 March 2018 CODEN: POLNC Correspondence Address: Mart{\'i}nez, C.; Centro de Estudios en Ciencia y Tecnolog{\'i}a de Alimentos (CECTA), Universidad de Santiago de Chile (USACH)Chile; email: claudio.martinez@usach.cl Chemicals/CAS: nitrogen, 7727-37-9 References: Querol, A., Fern{\'a}ndez-Espinar, M.T., Del Olmo, M., Barrio, E., Adaptive evolution of wine yeast (2003) Int J Food Microbiol, 86, pp. 3-10. , PMID: 12892918; Legras, J.L., Merdinoglu, D., Cornuet, J.M., Karst, F., Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history (2007) MolEcol, 16, pp. 2091-2102; Sicard, D., Legras, J.L., Bread, beer and wine: Yeast domestication in the Saccharomyces sensustricto complex (2001) C R Biol, 334, pp. 229-236; Cubillos, F.A., Billi, E., Zorgo, E., Parts, L., Fargier, P., Omholt, S., Assessing the complex architecture of polygenic traits in diverged yeast populations (2001) Mol Ecol, 20, pp. 1401-1413; Landry, C.R., Townsend, J.P., Hartl, D.L., Cavalieri, D., Ecological and evolutionary genomics of Saccharomyces cerevisiae (2006) Mol Ecol, 15, pp. 575-591. , https://doi.org/10.1111/j.1365-294X.2006.02778.x, PMID: 16499686; Hittinger, C.T., Saccharomyces diversity and evolution: A budding model genus (2013) Trends Genet, 29, pp. 309-317. , https://doi.org/10.1016/j.tig.2013.01.002, PMID: 23395329; Mortimer, R.K., Evolution and variation of the yeast (Saccharomyces) genome (2000) Genome Res, 10, pp. 403-409. , PMID: 10779481; Martini, A., Origin and domestication of the wine yeast Saccharomyces cerevisiae (1993) J Wine Res, 4, pp. 165-176; Naumov, G.I., Genetic identification of biological species in the Saccharomyces sensustricto complex (1996) J Ind Appl Microbiol, 17, pp. 295-302; Liti, G., Carter, D.M., Moses, A.M., Warringer, J., Parts, L., James, S.A., Population genomics of domestic and wild yeasts (2009) Nature, 458, pp. 337-341. , https://doi.org/10.1038/nature07743, PMID: 19212322; Fay, J.C., Benavides, J.A., Evidence for domesticated and wild populations of Saccharomyces cerevisiae (2005) PLoS Genet, 1, pp. 66-71. , https://doi.org/10.1371/journal.pgen.0010005, PMID: 16103919; Ibstedt, S., Stenberg, S., Bag{\'e}s, S., Gjuvsland, A.B., Salinas, F., Kourtchenko, O., Concerted evolution of life stage performances signals recent selection on yeast nitrogen use (2015) Mol Biol Evol, 32, pp. 153-161. , https://doi.org/10.1093/molbev/msu285, PMID: 25349282; Shen, F., Niu, X., Yang, D., Ying, Y., Li, B., Zhu, G., Determination of amino acids in Chinese rice wine by Fourier transform near-infrared spectroscopy (2010) Journal of Agricultural and Food Chemistry, 58, pp. 9809-9816. , https://doi.org/10.1021/jf1017912, PMID: 20707307; Yu, H., Zhang, Y., Xu, C., Tian, H., Discrimination of wine age of Chinese rice wine by electronic tongue based on amino acid profiles (2017) Transactions of Chinese Society of Agricultural Engineering, 33, pp. 297-301; Baker, H.G., Baker, I., Amino acids in nectar and their evolutionary significance (1973) Nature, 241, pp. 543-545; Gardener, M.C., Gillman, M.P., Analyzing variability in nectar amino acids: Composition is less variable than concentration (2001) J Chem Ecol, 27, pp. 2545-2558. , PMID: 11789958; Belly, M., Sablayrolles, J.M., Barre, P., Description of alcoholic fermentation kinetics: Its variability and significance (1990) Am. 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year = "2018",
doi = "10.1371/journal.pone.0192383",
language = "English",
volume = "13",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - Adaptability of the Saccharomyces cerevisiae yeasts to wine fermentation conditions relies on their strong ability to consume nitrogen

AU - Brice, C.

AU - Dequin, S.

AU - Camarasa, C.

AU - Cubillos Riffo, Francisco A.

AU - Cubillos Riffo, Francisco A.

AU - Martinez Fernandez, Claudio A.

AU - Martinez Fernandez, Claudio A.

N1 - Export Date: 26 March 2018 CODEN: POLNC Correspondence Address: Martínez, C.; Centro de Estudios en Ciencia y Tecnología de Alimentos (CECTA), Universidad de Santiago de Chile (USACH)Chile; email: claudio.martinez@usach.cl Chemicals/CAS: nitrogen, 7727-37-9 References: Querol, A., Fernández-Espinar, M.T., Del Olmo, M., Barrio, E., Adaptive evolution of wine yeast (2003) Int J Food Microbiol, 86, pp. 3-10. , PMID: 12892918; Legras, J.L., Merdinoglu, D., Cornuet, J.M., Karst, F., Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history (2007) MolEcol, 16, pp. 2091-2102; Sicard, D., Legras, J.L., Bread, beer and wine: Yeast domestication in the Saccharomyces sensustricto complex (2001) C R Biol, 334, pp. 229-236; Cubillos, F.A., Billi, E., Zorgo, E., Parts, L., Fargier, P., Omholt, S., Assessing the complex architecture of polygenic traits in diverged yeast populations (2001) Mol Ecol, 20, pp. 1401-1413; Landry, C.R., Townsend, J.P., Hartl, D.L., Cavalieri, D., Ecological and evolutionary genomics of Saccharomyces cerevisiae (2006) Mol Ecol, 15, pp. 575-591. , https://doi.org/10.1111/j.1365-294X.2006.02778.x, PMID: 16499686; Hittinger, C.T., Saccharomyces diversity and evolution: A budding model genus (2013) Trends Genet, 29, pp. 309-317. , https://doi.org/10.1016/j.tig.2013.01.002, PMID: 23395329; Mortimer, R.K., Evolution and variation of the yeast (Saccharomyces) genome (2000) Genome Res, 10, pp. 403-409. , PMID: 10779481; Martini, A., Origin and domestication of the wine yeast Saccharomyces cerevisiae (1993) J Wine Res, 4, pp. 165-176; Naumov, G.I., Genetic identification of biological species in the Saccharomyces sensustricto complex (1996) J Ind Appl Microbiol, 17, pp. 295-302; Liti, G., Carter, D.M., Moses, A.M., Warringer, J., Parts, L., James, S.A., Population genomics of domestic and wild yeasts (2009) Nature, 458, pp. 337-341. , https://doi.org/10.1038/nature07743, PMID: 19212322; Fay, J.C., Benavides, J.A., Evidence for domesticated and wild populations of Saccharomyces cerevisiae (2005) PLoS Genet, 1, pp. 66-71. , https://doi.org/10.1371/journal.pgen.0010005, PMID: 16103919; Ibstedt, S., Stenberg, S., Bagés, S., Gjuvsland, A.B., Salinas, F., Kourtchenko, O., Concerted evolution of life stage performances signals recent selection on yeast nitrogen use (2015) Mol Biol Evol, 32, pp. 153-161. , https://doi.org/10.1093/molbev/msu285, PMID: 25349282; Shen, F., Niu, X., Yang, D., Ying, Y., Li, B., Zhu, G., Determination of amino acids in Chinese rice wine by Fourier transform near-infrared spectroscopy (2010) Journal of Agricultural and Food Chemistry, 58, pp. 9809-9816. , https://doi.org/10.1021/jf1017912, PMID: 20707307; Yu, H., Zhang, Y., Xu, C., Tian, H., Discrimination of wine age of Chinese rice wine by electronic tongue based on amino acid profiles (2017) Transactions of Chinese Society of Agricultural Engineering, 33, pp. 297-301; Baker, H.G., Baker, I., Amino acids in nectar and their evolutionary significance (1973) Nature, 241, pp. 543-545; Gardener, M.C., Gillman, M.P., Analyzing variability in nectar amino acids: Composition is less variable than concentration (2001) J Chem Ecol, 27, pp. 2545-2558. , PMID: 11789958; Belly, M., Sablayrolles, J.M., Barre, P., Description of alcoholic fermentation kinetics: Its variability and significance (1990) Am. 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PY - 2018

Y1 - 2018

N2 - Saccharomyces cerevisiae strains are genetically diverse, largely as a result of human efforts to develop strains specifically adapted to various fermentation processes. These adaptive pressures from various ecological niches have generated behavioral differences among these strains, particularly in terms of their nitrogen consumption capacities. In this work, we characterize this phenotype by the specific quantity of nitrogen consumed under oenological fermentation conditions using a new approach. Indeed, unlike previous studies, our experiments were conducted in an environment containing excess nitrogen, eliminating the nitrogen limitation/starvation factor that is generally observed in fermentation processes. Using these conditions, we evaluated differences in the nitrogen consumption capacities for a set of five strains from diverse origins. The strains presented extremely different phenotypes and variations in their capacities to take up nitrogen from a wine fermentation environment. These variations reflect the differences in the nitrogen uptake capacities between wine and non-wine strains. Finally, the strains differed in their ability to adapt to the nitrogen composition of the environment, leading to variations in the cellular stress states, fermentation performances and the activity of the nitrogen sensing signaling pathway. © 2018 Brice et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

AB - Saccharomyces cerevisiae strains are genetically diverse, largely as a result of human efforts to develop strains specifically adapted to various fermentation processes. These adaptive pressures from various ecological niches have generated behavioral differences among these strains, particularly in terms of their nitrogen consumption capacities. In this work, we characterize this phenotype by the specific quantity of nitrogen consumed under oenological fermentation conditions using a new approach. Indeed, unlike previous studies, our experiments were conducted in an environment containing excess nitrogen, eliminating the nitrogen limitation/starvation factor that is generally observed in fermentation processes. Using these conditions, we evaluated differences in the nitrogen consumption capacities for a set of five strains from diverse origins. The strains presented extremely different phenotypes and variations in their capacities to take up nitrogen from a wine fermentation environment. These variations reflect the differences in the nitrogen uptake capacities between wine and non-wine strains. Finally, the strains differed in their ability to adapt to the nitrogen composition of the environment, leading to variations in the cellular stress states, fermentation performances and the activity of the nitrogen sensing signaling pathway. © 2018 Brice et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

KW - nitrogen

KW - Article

KW - cell culture

KW - cell stress

KW - comparative study

KW - controlled study

KW - evolutionary adaptation

KW - fermentation

KW - fungal strain

KW - gene library

KW - nitrogen uptake

KW - nonhuman

KW - phenotype

KW - RNA extraction

KW - RNA sequence

KW - Saccharomyces cerevisiae

KW - Saccharomyces cerevisiae 59A

KW - Saccharomyces cerevisiae A390D2

KW - Saccharomyces cerevisiae DBVPG6044

KW - Saccharomyces cerevisiae Y12

KW - Saccharomyces cerevisiae YPS128

KW - signal transduction

KW - starvation

KW - strain difference

KW - transcriptomics

KW - wine

U2 - 10.1371/journal.pone.0192383

DO - 10.1371/journal.pone.0192383

M3 - Article

VL - 13

JO - PLoS One

T2 - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 2

ER -