Microbial Communities of Flor Velums and the Genetic Stability of Flor Yeasts Used for a Long Time for the Industrial Production of Sherry-like Wines

Andrey V. Mardanov; Eugeny V. Gruzdev; Alexey V. Beletsky; Elena V. Ivanova; Maksim Yu. Shalamitskiy; Tatiana N. Tanashchuk; Nikolai V. Ravin

doi:10.3390/fermentation9040367

journal article Open Access Apr 09, 2023

Microbial Communities of Flor Velums and the Genetic Stability of Flor Yeasts Used for a Long Time for the Industrial Production of Sherry-like Wines

Andrey V. Mardanov

Eugeny V. Gruzdev Alexey V. Beletsky Elena V. Ivanova Maksim Yu. Shalamitskiy

Tatiana N. Tanashchuk Nikolai V. Ravin

Fermentation Vol. 9 No. 4 pp. 367 · MDPI AG

View at Publisher Save 10.3390/fermentation9040367

Abstract

Flor yeast strains represent a specialized group of Saccharomyces cerevisiae yeasts used for the production of sherry-like wines by biological wine aging. We sequenced the genome of the industrial flor yeast strain I-329 from a collection of microorganisms for winemaking “Magarach” and the metagenomes of two flor velums based on this strain and continuously maintained for several decades. The winery uses two processes for the production of sherry-like wine: batch aging and a continuous process similar to the criaderas–solera system. The 18S rRNA gene profiling and sequencing of metagenomes of flor velums revealed the presence of the yeasts Pichia membranifaciens and Malassezia restricta in minor amounts along with the dominant S. cerevisiae I-329 flor yeast. Bacteria Oenococcus oeni and Lentilactobacillus hilgardii together accounted for approximately 20% of the velum microbiota in the case of a batch process, but less than 1% in the velum used in the continuous process. Collection strain I-329 was triploid for all chromosomes except diploid chromosomes I and III, while the copy numbers of all chromosomes were equal in industrial velums. A comparative analysis of the genome of strain I-329 maintained in the collection and metagenomes of industrial velums revealed only several dozens of single nucleotide polymorphisms, which indicates a long-term genetic stability of this flor yeast strain under the harsh conditions of biological wine aging.

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References

67

[1]

Collin "Main odorants in Jura flor-sherry wines. Relative contributions of sotolon, abhexon, and theaspirane-derived compounds" J. Agric. Food Chem. (2012) 10.1021/jf203832c

[2]

Zea "Acetaldehyde as key compound for the authenticity of sherry wines: A study covering 5 decades" Compr. Rev. Food Sci. Food Saf. (2015) 10.1111/1541-4337.12159

[3]

Durán-Guerrero, E., Castro, R., García-Moreno, M.d.V., Rodríguez-Dodero, M.d.C., Schwarz, M., and Guillén-Sánchez, D. (2021). Aroma of Sherry Products: A Review. Foods, 10. 10.3390/foods10040753

[4]

Rodriguez "Evolution of flor yeast population during the biological aging of fino sherry wine" Am. J. Enol. Vitic. (1997) 10.5344/ajev.1997.48.2.160

[5]

Coi "Genomic signatures of adaptation to wine biological ageing conditions in biofilm-forming flor yeasts" Mol. Ecol. (2017) 10.1111/mec.14053

[6]

Legras "Flor yeast: New perspectives beyond wine aging" Front. Microbiol. (2016) 10.3389/fmicb.2016.00503

[7]

Eldarov "Whole-genome analysis of three yeast strains used for production of sherry-like wines revealed genetic traits specific to flor yeasts" Fron. Microbiol. (2018) 10.3389/fmicb.2018.00965

[8]

Sipiczki "Diversity, variability and fast adaptive evolution of the wine yeast (Saccharomyces cerevisiae) genome—A review" Ann. Microbiol. (2011) 10.1007/s13213-010-0086-4

[9]

Peter "Genome evolution across 1011 Saccharomyces cerevisiae isolates" Nature (2018) 10.1038/s41586-018-0030-5

[10]

Legras, J.L., Erny, C., and Charpentier, C. (2014). Population structure and comparative genome hybridization of European flor yeast reveal a unique group of Saccharomyces cerevisiae strains with few gene duplications in their genome. PLoS ONE, 9. 10.1371/journal.pone.0108089

[11]

Morard "Aneuploidy and ethanol tolerance in Saccharomyces cerevisiae" Front. Genet. (2019) 10.3389/fgene.2019.00082

[12]

Voordeckers, K., Kominek, J., Das, A., Espinosa-Cantu, A., De Maeyer, D., Arslan, A., Van Pee, M., van der Zande, E., Meert, W., and Yang, Y. (2015). Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet., 11. 10.1371/journal.pgen.1005635

[13]

Yona "Chromosomal duplication is a transient evolutionary solution to stress" Proc. Natl. Acad. Sci. USA (2012) 10.1073/pnas.1211150109

[14]

Gilchrist "Aneuploidy in yeast: Segregation error or adaptation mechanism?" Yeast (2019) 10.1002/yea.3427

[15]

Legras "Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication" Mol. Biol. Evol. (2018) 10.1093/molbev/msy066

[16]

Coi "Study of the role of the covalently linked cell wall protein (Ccw14p) and yeast glycoprotein (Ygp1p) within biofilm formation in a flor yeast strain" FEMS Yeast Res. (2018)

[17]

Fidalgo "Adaptive evolution by mutations in the FLO11 gene" Proc. Natl. Acad. Sci. USA (2006) 10.1073/pnas.0601713103

[18]

Zara "FLO11-based model for air-liquid interfacial biofilm formation by Saccharomyces cerevisiae" Appl. Environ. Microbiol. (2005) 10.1128/aem.71.6.2934-2939.2005

[19]

Zara "FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae" Microbiology (2009) 10.1099/mic.0.028738-0

[20]

Cantoral "Rethinking about flor yeast diversity and its dynamic in the “criaderas and soleras” biological aging system" Food Microbiol. (2020) 10.1016/j.fm.2020.103553

[21]

Vicente, J., Calderón, F., Santos, A., Marquina, D., and Benito, S. (2021). High Potential of Pichia kluyveri and other Pichia species in Wine technology. Int. J. Mol. Sci., 22. 10.3390/ijms22031196

[22]

Moreno "Revealing the yeast diversity of the flor biofilm microbiota in sherry wines through internal transcribed spacer-metabarcoding and matrix-assisted laser desorption/ionization time of flight mass spectrometry" Front. Microbiol. (2022) 10.3389/fmicb.2021.825756

[23]

Kishkovskaia "Flor yeast strains from culture collection: Genetic diversity and physiological and biochemical properties" Appl. Biochem. Microbiol. (2017) 10.1134/s0003683817030085

[24]

Ristow "Chromosomal damages by ethanol and acetaldehyde in Saccharomyces cerevisiae as studied by pulsed field gel electrophoresis" Mutat. Res. (1995) 10.1016/0027-5107(94)00165-2

[25]

International Organization of Vine and Wine (2022). Compendium of International Methods of Wine and Must Analysis, O.I.V.

[26]

Bass "Coprophilic amoebae and flagellates, including Guttulinopsis, Rosculus and Helkesimastix, characterise a divergent and diverse rhizarian radiation and contribute to a large diversity of faecal-associated protists" Environ. Microbiol. (2016) 10.1111/1462-2920.13235

[27]

FLASH: fast length adjustment of short reads to improve genome assemblies

Tanja Magoč, Steven L. Salzberg

Bioinformatics 2011 10.1093/bioinformatics/btr507

[28]

Search and clustering orders of magnitude faster than BLAST

Robert C. Edgar

Bioinformatics 2010 10.1093/bioinformatics/btq461

[29]

Sreenivasaprasad, S. (2000). The Nucleic Acid Protocols Handbook, Humana Press.

[30]

Wick, R.R., Judd, L.M., Gorrie, C.L., and Holt, K.E. (2017). Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol., 13. 10.1371/journal.pcbi.1005595

[31]

Gene and translation initiation site prediction in metagenomic sequences

Doug Hyatt, Philip F. LoCascio, Loren J. Hauser et al.

Bioinformatics 2012 10.1093/bioinformatics/bts429

[32]

Uniclust databases of clustered and deeply annotated protein sequences and alignments

Milot Mirdita, Lars von den Driesch, Clovis Galiez et al.

Nucleic Acids Research 2017 10.1093/nar/gkw1081

[33]

Fast and sensitive protein alignment using DIAMOND

Benjamin Buchfink, Chao Xie, Daniel H Huson

Nature Methods 2015 10.1038/nmeth.3176

[34]

Buchfink "Sensitive protein alignments at tree-of-life scale using DIAMOND" Nat. Methods (2021) 10.1038/s41592-021-01101-x

[35]

KEGG for linking genomes to life and the environment

M. Kanehisa, M. Araki, S. Goto et al.

Nucleic Acids Research 2008 10.1093/nar/gkm882

[36]

Zhou "METABOLIC: High-throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community-scale functional networks" Microbiome (2022) 10.1186/s40168-021-01213-8

[37]

Cutadapt removes adapter sequences from high-throughput sequencing reads

Marcel Martin

EMBnet.journal 2011 10.14806/ej.17.1.200

[38]

Prjibelski "Using SPAdes de novo assembler" Curr. Protoc. Bioinform. (2020) 10.1002/cpbi.102

[39]

Kang "MetaBAT 2: An adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies" PeerJ (2019) 10.7717/peerj.7359

[40]

MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm

Yu-Wei Wu, Yung-Hsu Tang, Susannah G Tringe et al.

Microbiome 2014 10.1186/2049-2618-2-26

[41]

Binning metagenomic contigs by coverage and composition

Johannes Alneberg, Brynjar Smári Bjarnason, Ino de Bruijn et al.

Nature Methods 2014 10.1038/nmeth.3103

[42]

Sieber "Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy" Nat. Microbiol. (2018) 10.1038/s41564-018-0171-1

[43]

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes

Donovan H. Parks, Michael Imelfort, Connor T. Skennerton et al.

Genome Research 2015 10.1101/gr.186072.114

[44]

GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database

Pierre-Alain Chaumeil, Aaron J Mussig, Philip Hugenholtz et al.

Bioinformatics 2019 10.1093/bioinformatics/btz848

[45]

Parks "GTDB: An ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy" Nucleic Acids Res. (2022) 10.1093/nar/gkab776

[46]

Fast gapped-read alignment with Bowtie 2

Ben Langmead, Steven L Salzberg

Nature Methods 2012 10.1038/nmeth.1923

[47]

Garrison, E., and Marth, G. (2012). Haplotype-based variant detection from short-read sequencing. arXiv.

[48]

Veiga "Effects of weak acid preservatives on the growth and thermal death of the yeast Pichia membranifaciens in a commercial apple juice" Int. J. Food Microbiol. (2000) 10.1016/s0168-1605(99)00191-9

[49]

Doijad "Antimicrobial Activity of a Novel Pichia membranifaciens Strain Isolated from Naturally Fermented Cashew Apple Juice" Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. (2016) 10.1007/s40011-014-0417-5

[50]

Belda, I., Ruiz, J., Alonso, A., Marquina, D., and Santos, A. (2017). The biology of Pichia membranifaciens killer toxins. Toxins, 9. 10.3390/toxins9040112

Showing 50 of 67 references

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Details

Published: Apr 09, 2023
Vol/Issue: 9(4)
Pages: 367
License: View

Authors

A

Andrey V. Mardanov

Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, 119071 Moscow, Russia

E

Eugeny V. Gruzdev

Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, 119071 Moscow, Russia

A

Alexey V. Beletsky

Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, 119071 Moscow, Russia

E

Elena V. Ivanova

All-Russian National Research Institute of Viticulture and Winemaking “Magarach”, Russian Academy of Sciences, 298600 Yalta, Russia

M

Maksim Yu. Shalamitskiy

All-Russian National Research Institute of Viticulture and Winemaking “Magarach”, Russian Academy of Sciences, 298600 Yalta, Russia

T

Tatiana N. Tanashchuk

All-Russian National Research Institute of Viticulture and Winemaking “Magarach”, Russian Academy of Sciences, 298600 Yalta, Russia

N

Nikolai V. Ravin

Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, 119071 Moscow, Russia

Funding

Ministry of Science and Higher Education of the Russian Federation Award: 075-15-2022-318

Cite This Article

Andrey V. Mardanov, Eugeny V. Gruzdev, Alexey V. Beletsky, et al. (2023). Microbial Communities of Flor Velums and the Genetic Stability of Flor Yeasts Used for a Long Time for the Industrial Production of Sherry-like Wines. Fermentation, 9(4), 367. https://doi.org/10.3390/fermentation9040367

Microbial Communities of Flor Velums and the Genetic Stability of Flor Yeasts Used for a Long Time for the Industrial Production of Sherry-like Wines

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