Enhanced flavour profiles through radicicol induced genomic variation in the lager yeasts, Saccharomyces pastorianus.


Journal

Yeast (Chichester, England)
ISSN: 1097-0061
Titre abrégé: Yeast
Pays: England
ID NLM: 8607637

Informations de publication

Date de publication:
10 2022
Historique:
revised: 13 09 2022
received: 24 06 2022
accepted: 15 09 2022
pubmed: 22 9 2022
medline: 12 10 2022
entrez: 21 9 2022
Statut: ppublish

Résumé

The yeasts, Saccharomyces pastorianus, are hybrids of Saccharomyces cerevisiae and Saccharomyces eubayanus and have acquired traits from the combined parental genomes such as ability to ferment a range of sugars at low temperatures and to produce aromatic flavour compounds, allowing for the production of lager beers with crisp, clean flavours. The polyploid strains are sterile and have reached an evolutionary bottleneck for genetic variation. Here we describe an accelerated evolution approach to obtain lager yeasts with enhanced flavour profiles. As the relative expression of orthologous alleles is a significant contributor to the transcriptome during fermentation, we aimed to induce genetic variation by altering the S. cerevisiae to S. eubayanus chromosome ratio. Aneuploidy was induced through the temporary inhibition of the cell's stress response and strains with increased production of aromatic amino acids via the Shikimate pathway were selected by resistance to amino acid analogues. Genomic changes such as gross chromosomal rearrangements, chromosome loss and chromosome gain were detected in the characterised mutants, as were single-nucleotide polymorphisms in ARO4, encoding for DAHP synthase, the catalytic enzyme in the first step of the Shikimate pathway. Transcriptome analysis confirmed the upregulation of genes encoding enzymes in the Ehrlich pathway and the concomitant increase in the production of higher alcohols and esters such as 2-phenylethanol, 2-phenylethyl acetate, tryptophol, and tyrosol. We propose that the polyploid nature of S. pastorianus genomes is an advantageous trait supporting opportunities for genetic alteration in otherwise sterile strains.

Identifiants

pubmed: 36127846
doi: 10.1002/yea.3815
doi:

Substances chimiques

3-Deoxy-7-Phosphoheptulonate Synthase EC 2.5.1.54
Amino Acids 0
Amino Acids, Aromatic 0
Macrolides 0
monorden I60EH8GECX
Phenylethyl Alcohol ML9LGA7468
Sugars 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

535-547

Subventions

Organisme : Marie Curie
ID : 764364
Pays : United Kingdom

Informations de copyright

© 2022 The Authors. Yeast published by John Wiley & Sons Ltd.

Références

Baker, E., Wang, B., Bellora, N., Peris, D., Hulfachor, A. B., Koshalek, J. A., Adams, M., Libkind, D., & Hittinger, C. T. (2015). The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Molecular Biology and Evolution, 32(11), 2818-2831. https://doi.org/10.1093/molbev/msv168
Beggs, S., James, T. C., & Bond, U. (2012). The PolyA tail length of yeast histone mRNAs varies during the cell cycle and is influenced by Sen1p and Rrp6p. Nucleic Acids Research, 40(6), 2700-2711. https://doi.org/10.1093/nar/gkr1108
Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W. H., Pagès, F., Trajanoski, Z., & Galon, J. (2009). ClueGO: A Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics, 25(8), 1091-1093. https://doi.org/10.1093/bioinformatics/btp101
Bond, U., Neal, C., Donnelly, D., & James, T. C. (2004). Aneuploidy and copy number breakpoints in the genome of lager yeasts mapped by microarray hybridisation. Current Genetics, 45(6), 360-370. https://doi.org/10.1007/s00294-004-0504-x
Bozdag, G.O., Ono, J., Denton, J.A., Karakoc, E., Hunter, N., Leu, J. Y., & Greig, D. (2021). Breaking a species barrier by enabling hybrid recombination. Current Biology 31(4), R180-R181. https://doi.org/10.1016/j.cub.2020.12.038
Brouwers, N., Brickwedde, A., Gorter de Vries, A. R., van den Broek, M., Weening, S. M., van den Eijnden, L., Diderich, J. A., Bai, F. Y., Pronk, J. T., & Daran, J. M. G. (2019). Himalayan Saccharomyces eubayanus genome sequences reveal genetic markers explaining heterotic maltotriose consumption by Saccharomyces pastorianus hybrids. Applied and Environmental Microbiology, 85(22), e01516-19. https://doi.org/10.1128/AEM.01516-19
Chen, G., Bradford, W. D., Seidel, C. W., & Li, R. (2012). Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy. Nature, 482(7384), 246-250. https://doi.org/10.1038/nature10795
Cordente, A. G., Solomon, M., Schulkin, A., Leigh Francis, I., Barker, A., Borneman, A. R., & Curtin, C. D. (2018). Novel wine yeast with ARO4 and TYR1 mutations that overproduce ‘floral’ aroma compounds 2-phenylethanol and 2-phenylethyl acetate. Applied Microbiology and Biotechnology, 102(14), 5977-5988. https://doi.org/10.1007/s00253-018-9054-x
De la cerda garcia-Caro, R., Hokamp, K., Roche, F., Thompson, G., Timouma, S., Delneri, D., & Bond, U. (2022). Aneuploidy influences the gene expression profiles in Saccharomyces pastorianus group I and II strains during fermentation. PLoS Genetics, 18(4), e1010149. https://doi.org/10.1371/journal.pgen.1010149
Di Benedetto, R., Varì, R., Scazzocchio, B., Filesi, C., Santangelo, C., Giovannini, C., Matarrese, P., D'Archivio, M., & Masella, R. (2007). Tyrosol, the major extra virgin olive oil compound, restored intracellular antioxidant defences in spite of its weak antioxidative effectiveness. Nutrition, Metabolism, and Cardiovascular Diseases, 17(7), 535-545. https://doi.org/10.1016/j.numecd.2006.03.005
Dietvorst, J., Londesborough, J., & Steensma, H. Y. (2005). Maltotriose utilization in lager yeast strains: MTT1 encodes a maltotriose transporter. Yeast, 22(10), 775-788. https://doi.org/10.1002/yea.1279
Dietvorst, J., Walsh, M. C., van Heusden, G.P.H., & Steensma, H. Y. (2010). Comparison of the MTT1- and MAL31-like maltose transporter genes in lager yeast strains. FEMS Microbiology Letters, 310(2), 152-157. https://doi.org/10.1111/j.1574-6968.2010.02056.x
Dunn, B., Richter, C., Kvitek, D. J., Pugh, T., & Sherlock, G. (2012). Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Research, 22(5), 908-924. https://doi.org/10.1101/gr.130310.111
Dunn, B. & Sherlock, G. (2008). Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Research, 18(10), 1610-1623. https://doi.org/10.1101/gr.076075.108
Dzialo, M. C., Park, R., Steensels, J., Lievens, B., & Verstrepen, K. J. (2017). Physiology, ecology and industrial applications of aroma formation in yeast. FEMS Microbiology Reviews, 41(Supp_1), S95-S128. https://doi.org/10.1093/femsre/fux031
Ge, S. X., Son, E. W., & Yao, R. (2018). iDEP: An integrated web application for differential expression and pathway analysis of RNA-Seq data. BMC Bioinformatics, 19(1), 534. https://doi.org/10.1186/s12859-018-2486-6
Gibson, B. R., Storgårds, E., Krogerus, K., & Vidgren, V. (2013). Comparative physiology and fermentation performance of Saaz and Frohberg lager yeast strains and the parental species Saccharomyces eubayanus. Yeast, 30(7), 255-266. https://doi.org/10.1002/yea.2960
Gorter de Vries, A. R., Knibbe, E., van Roosmalen, R., van den Broek, M., de la Torre Cortés, P., O'Herne, S. F., Vijverberg, P. A., El Masoudi, A., Brouwers, N., Pronk, J. T., & Daran, J. M. G. (2020). Improving industrially relevant phenotypic traits by engineering chromosome copy number in Saccharomyces pastorianus. Frontiers in Genetics, 11, 518. https://doi.org/10.3389/fgene.2020.00518
Gorter de Vries, A. R., Voskamp, M. A., van Aalst, A. C. A., Kristensen, L. H., Jansen, L., van den Broek, M., Salazar, A. N., Brouwers, N., Abeel, T., Pronk, J. T., & Daran, J. M. G. (2019). Laboratory evolution of a Saccharomyces cerevisiae × S. eubayanus hybrid under simulated Lager-Brewing conditions. Frontiers in Genetics, 10, 242. https://doi.org/10.3389/fgene.2019.00242
Hartmann, M., Schneider, T. R., Pfeil, A., Heinrich, G., Lipscomb, W. N., & Braus, G. H. (2003). Evolution of feedback-inhibited β/α barrel isoenzymes by gene duplication and a single mutation. Proceedings of the National Academy of Sciences of the United States of America, 100(3), 862-867. https://doi.org/10.1073/pnas.0337566100
Hebly, M., Brickwedde, A., Bolat, I., Driessen, M. R. M., de Hulster, E. A. F., van den Broek, M., Pronk, J. T., Geertman, J. M., Daran, J. M., & Daran-Lapujade, P. (2015). S. cerevisiae × S. eubayanus interspecific hybrid, the best of both worlds and beyond. FEMS Yeast Research, 15(3), fov005. https://doi.org/10.1093/femsyr/fov005
Hewitt, S. K., Donaldson, I. J., Lovell, S. C., & Delneri, D. (2014). Sequencing and characterisation of rearrangements in three S. pastorianus strains reveals the presence of chimeric genes and gives evidence of breakpoint reuse. PLoS One, 9(3), e92203. https://doi.org/10.1371/journal.pone.0092203
James, T. C., Usher, J., Campbell, S., & Bond, U. (2008). Lager yeasts possess dynamic genomes that undergo rearrangements and gene amplification in response to stress. Current Genetics, 53(3), 139-152. https://doi.org/10.1007/s00294-007-0172-8
Krogerus, K., Magalhães, F., Castillo, S., Peddinti, G., Vidgren, V., De Chiara, M., Yue, J. X., Liti, G., & Gibson, B. (2021). Lager yeast design through meiotic segregation of a Saccharomyces cerevisiae × Saccharomyces eubayanus hybrid. Frontiers in Fungal Biology, 2, 733655. https://doi.org/10.3389/ffunb.2021.733655
Krogerus, K., Seppänen-Laakso, T., Castillo, S., & Gibson, B. (2017). Inheritance of brewing-relevant phenotypes in constructed Saccharomyces cerevisiae × Saccharomyces eubayanus hybrids. Microbial Cell Factories, 16(1), 66. https://doi.org/10.1186/s12934-017-0679-8
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357-359. https://doi.org/10.1038/nmeth.1923
Lin, C. L., García-Caro, R. C., Zhang, P., Carlin, S., Gottlieb, A., Petersen, M. A., Vrhovsek, U., & Bond, U. (2021). Packing a punch: Understanding how flavours are produced in lager fermentations. FEMS Yeast Research, 21(5), foab040. https://doi.org/10.1093/femsyr/foab040
Mertens, S., Steensels, J., Saels, V., De Rouck, G., Aerts, G., & Verstrepen, K. J. (2015). A large set of newly created interspecific Saccharomyces hybrids increases aromatic diversity in lager beers. Applied and Environmental Microbiology, 81(23), 8202-8214. https://doi.org/10.1128/AEM.02464-15
Monerawela, C., & Bond, U. (2017). Brewing up a storm: The genomes of lager yeasts and how they evolved. Biotechnology Advances, 35(4), 512-519. https://doi.org/10.1016/j.biotechadv.2017.03.003
Monerawela, C., & Bond, U. (2018). The hybrid genomes of Saccharomyces pastorianus: A current perspective. Yeast, 35(1), 39-50. https://doi.org/10.1002/yea.3250
Naseeb, S., James, S. A., Alsammar, H., Michaels, C. J., Gini, B., Nueno-Palop, C., Bond, C. J., McGhie, H., Roberts, I. N., & Delneri, D. (2017). Saccharomyces jurei sp. nov., isolation and genetic identification of a novel yeast species from Quercus robur. International Journal of Systematic and Evolutionary Microbiology, 67(6), 2046-2052. https://doi.org/10.1099/ijsem.0.002013
Okuno, M., Kajitani, R., Ryusui, R., Morimoto, H., Kodama, Y., & Itoh, T. (2016). Next-generation sequencing analysis of lager brewing yeast strains reveals the evolutionary history of interspecies hybridization. DNA Research, 23(1), dsv037. https://doi.org/10.1093/dnares/dsv037
Pennisi, R., Ascenzi, P., & di Masi, A. (2015). Hsp90: A new player in DNA repair? Biomolecules, 5(4), 2589-2618. https://doi.org/10.3390/biom5042589
Pérez-Torrado, R., Querol, A., & Guillamón, J. M. (2015). Genetic improvement of non-GMO wine yeasts: Strategies, advantages and safety. Trends in Food Science & Technology, 45(1), 1-11. https://doi.org/10.1016/j.tifs.2015.05.002
Piatkowska, E. M., Naseeb, S., Knight, D., & Delneri, D. (2013). Chimeric protein complexes in hybrid species generate novel phenotypes. PLoS Genetics, 9(10), e1003836. https://doi.org/10.1371/journal.pgen.1003836
Querol, A., Barrio, E., & Ramón, D. (1992). A comparative study of different methods of yeast strain characterization. Systematic and Applied Microbiology, 15(3), 439-446. https://doi.org/10.1016/s0723-2020(11)80219-5
Rebollo-Romero, I., Fernández-Cruz, E., Carrasco-Galán, F., Valero, E., Cantos-Villar, E., Cerezo, A. B., Troncoso, A. M., & Garcia-Parrilla, M. C. (2020). Factors influencing the production of the antioxidant hydroxytyrosol during alcoholic fermentation: Yeast strain, initial tyrosine concentration and initial must. Lwt, 130, 109631. https://doi.org/10.1016/j.lwt.2020.109631
Salazar, A. N., Gorter de Vries, A. R., van den Broek, M., Brouwers, N., de la Torre Cortès, P., Kuijpers, N. G. A., Daran, J. M. G., & Abeel, T. (2019). Chromosome level assembly and comparative genome analysis confirm lager-brewing yeasts originated from a single hybridization. BMC Genomics, 20(1), 916. https://doi.org/10.1186/s12864-019-6263-3
Škrab, D., Sivilotti, P., Comuzzo, P., Voce, S., Degano, F., Carlin, S., Arapitsas, P., Masuero, D., & Vrhovšek, U. (2021). Cluster thinning and vineyard site modulate the metabolomic profile of Ribolla Gialla base and sparkling wines. Metabolites, 11, (5), 331. https://doi.org/10.3390/metabo11050331
Soejima, H., Tsuge, K., Yoshimura, T., Sawada, K., & Kitagaki, H. (2012). Breeding of a high tyrosol-producing sake yeast by isolation of an ethanol-resistant mutant from atrp3mutant. Journal of the Institute of Brewing, 118(3), 264-268. https://doi.org/10.1002/jib.46
Strejc, J., Siříšťová, L., Karabín, M., Almeida e Silva, J. B., & Brányik, T. (2013). Production of alcohol-free beer with elevated amounts of flavouring compounds using lager yeast mutants. Journal of the Institute of Brewing, 119(3), 149-155. https://doi.org/10.1002/jib.72
Thorvaldsdottir, H., Robinson, J. T., & Mesirov, J. P. (2013). Integrative genomics viewer (IGV): High-performance genomics data visualization and exploration. Briefings in Bioinformatics, 14(2), 178-192. https://doi.org/10.1093/bib/bbs017
Timouma, S., Balarezo-Cisneros, L. N., Pinto, J., De La Cerda, R., Bond, U., Schwartz, J. M., & Delneri, D. (2021). Transcriptional profile of the industrial hybrid Saccharomyces pastorianus reveals temperature-dependent allele expression bias and preferential orthologous protein assemblies. Molecular Biology and Evolution, 38, 5437-5452. https://doi.org/10.1093/molbev/msab282
Trepel, J., Mollapour, M., Giaccone, G., & Neckers, L. (2010). Targeting the dynamic HSP90 complex in cancer. Nature Reviews Cancer, 10(8), 537-549. https://doi.org/10.1038/nrc2887
Vidgren, V., & Gibson, B. (2018). Trans-regulation and localization of orthologous maltose transporters in the interspecies lager yeast hybrid. FEMS Yeast Research, 18(6), foy065. https://doi.org/10.1093/femsyr/foy065
Vidgren, V., Ruohonen, L., & Londesborough, J. (2005). Characterization and functional analysis of the MAL and MPH Loci for maltose utilization in some ale and lager yeast strains. Applied and Environmental Microbiology, 71(12), 7846-7857. https://doi.org/10.1128/AEM.71.12.7846-7857.2005
Wang, K., Li, M., & Hakonarson, H. (2010). ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Research, 38(16), e164. https://doi.org/10.1093/nar/gkq603

Auteurs

Roberto de la Cerda Garcia-Caro (R)

Department of Microbiology, School of Genetics and Microbiology, Moyne Institute, Trinity College Dublin, Dublin, Ireland.

Georgia Thompson (G)

Department of Microbiology, School of Genetics and Microbiology, Moyne Institute, Trinity College Dublin, Dublin, Ireland.

Penghan Zhang (P)

Metabolomic Unit, Food Quality and Nutrition Department, Research and Innovation Centre, Edmund Mach Foundation, Michele all'Adige, Italy.

Karsten Hokamp (K)

Department of Genetics, School of Genetics and Microbiology, Smurfit Institute, Trinity College Dublin, Dublin, Ireland.

Fiona Roche (F)

Department of Genetics, School of Genetics and Microbiology, Smurfit Institute, Trinity College Dublin, Dublin, Ireland.

Silvia Carlin (S)

Metabolomic Unit, Food Quality and Nutrition Department, Research and Innovation Centre, Edmund Mach Foundation, Michele all'Adige, Italy.

Urska Vrhovsek (U)

Metabolomic Unit, Food Quality and Nutrition Department, Research and Innovation Centre, Edmund Mach Foundation, Michele all'Adige, Italy.

Ursula Bond (U)

Department of Microbiology, School of Genetics and Microbiology, Moyne Institute, Trinity College Dublin, Dublin, Ireland.

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Classifications MeSH