1. Pasteur, L. Nouvelles expériences pour démontrer que le germe de la levure qui fait le vin provient de l’extérieur des grains de
raisin. C. R. Acad. Sci. 75, 781–793 (1872).
2. Mortimer, R. & Polsinelli, M. On the origins of wine yeast. Res. Microbiol. 150, 199–204 (1999).
3. Barata, A., Malfeito-Ferreira, M. & Loureiro, V. The microbial ecology of wine grape berries. Int. J. Food Microbiol. 153, 243–259
(2012).
4. Loureiro, V., Ferreira, M. M., Monteiro, S. & Ferreira, R. B. The microbial community of grape berry. In The Biochemistry of the
Grape Berry (eds Gerós, H. et al.) 241–268 (Bentham Science, 2012).
5. Goddard, M. R. & Greig, D. Saccharomyces cerevisiae: A nomadic yeast with no niche?. FEMS Yeast Res. 15, fov009 (2015).
6. Lleixà, J., Kioroglou, D., Mas, A. & Portillo, M. D. C. Microbiome dynamics during spontaneous fermentations of sound grapes
in comparison with sour rot and Botrytis infected grapes. Int. J. Food Microbiol. 281, 36–46 (2018).
7. Mezzasalma, V. et al. Geographical and cultivar features differentiate grape microbiota in Northern Italy and Spain vineyards.
Front. Microbiol. 9, 946 (2018).
8. Stefanini, I. & Cavalieri, D. Metagenomic approaches to investigate the contribution of the vineyard environment to the quality
of wine fermentation: Potentials and difficulties. Front. Microbiol. 9, 991 (2018).
9. Vitulo, N. et al. Bark and grape microbiome of Vitis vinifera: influence of geographic patterns and agronomic management on
bacterial diversity. Front. Microbiol. 9, 3203 (2019).
10. Stefanini, I. et al. Role of social wasps in Saccharomyces cerevisiae ecology and evolution. Proc. Natl. Acad. Sci. USA 109, 13398–
13403 (2012).
11. Francesca, N. et al. Yeasts vectored by migratory birds collected in the Mediterranean island of Ustica and description of Phaffomyces usticensis f.a. sp. Nov., a new species related to the cactus ecoclade. FEMS Yeast Res. 14, 910–921 (2014).
12. Wang, X.-C. et al. Evaluation of aroma enhancement for “Ecolly” dry white wines by mixed inoculation of selected Rhodotorula
mucilaginosa and Saccharomyces cerevisiae. Food Chem. 228, 550–559 (2017).
13. Merín, M. G. & de Ambrosini, V. I. M. Kinetic and metabolic behaviour of the pectinolytic strain Aureobasidium pullulans GM-R22 during pre-fermentative cold maceration and its effect on red wine quality. Int. J. Food Microbiol. 285, 18–26 (2018).
14. Onetto, C. A., Borneman, A. R. & Schmidt, S. A. Investigating the effects of Aureobasidium pullulans on grape juice composition
and fermentation. Food Microbiol. 90, 103451 (2020).
15. Gao, Y., Zietsman, A. J. J., Vivier, M. A. & Moore, J. P. Deconstructing wine grape cell walls with enzymes during winemaking:
new insights from glycan microarray technology. Molecules 24, 165 (2019).
16. Martínez-Lapuente, L., Guadalupe, Z., Ayestarán, B. Properties of wine polysaccharides. In: Masuelli, M. (ed.). Pectins - Extraction,
Purification, Characterization and Applications. IntechOpen. 2019. https://doi.org/10.5772/intechopen.85629.
17. Lecas, M. & Brillouet, J.-M. Cell wall composition of grape berry skins. Phytochemistry 35, 1241–1243 (1994).
18. González-Centeno, M. R. et al. Physico-chemical properties of cell wall materials obtained from ten grape varieties and their
byproducts: Grape pomaces and stems. LWT Food Sci. Technol. 43, 1580–1586 (2010).
19. Biely, P., Heinrichová, K. & Kružiková, M. Induction and inducers of the pectolytic system in Aureobasidium pullulans. Curr.
Microbiol. 33, 6–10 (1996).
20. Strauss, M. L., Jolly, N. P., Lambrechts, M. G. & van Rensburg, P. Screening for the production of extracellular hydrolytic enzymes
by non-Saccharomyces wine yeasts. J. Appl. Microbiol. 91, 182–190 (2001).
21. Merín, M. G., Mendoza, L. M., Farías, M. E. & Morata de Ambrosini, V. I. Isolation and selection of yeasts from wine grape ecosystem secreting cold-active pectinolytic activity. Int. J. Food Microbiol. 147, 144–148 (2011).
22. Úbeda, J., Maldonado Gil, M., Chiva, R., Guillamón, J. M. & Briones, A. Biodiversity of non-Saccharomyces yeasts in distilleries
of the La Mancha region (Spain). FEMS Yeast Res. 14, 663–673 (2014).
Scientific Reports |
(2023) 13:9279 |
https://doi.org/10.1038/s41598-023-35734-z
11
Vol.:(0123456789)
www.nature.com/scientificreports/
23. Huisjes, E. H. et al. Toward pectin fermentation by Saccharomyces cerevisiae: Expression of the first two steps of a bacterial pathway
for d-galacturonate metabolism. J. Biotechnol. 162, 303–331 (2012).
24. Casa-Villegas, M., Polaina, J. & Marín-Navarro, J. Cellobiose fermentation by Saccharomyces cerevisiae: Comparative analysis of
intra versus extracellular sugar hydrolysis. Process. Biochem. 75, 59–67 (2018).
25. Domínguez, E., Heredia-Guerrero, J. A. & Heredia, A. The biophysical design of plant cuticles: An overview. New Phytol. 189,
938–949 (2011).
26. Martin, L. B. B. & Rose, J. K. C. There’s more than one way to skin a fruit: Formation and functions of fruit cuticles. J. Exp. Bot. 65,
4639–4651 (2014).
27. Ziv, C., Zhao, Z., Gao, Y. G. & Xia, Y. Multifunctional roles of plant cuticle during plant-pathogen interactions. Front. Plant Sci. 9,
1088 (2018).
28. Egmond, M. R. & de Vlieg, J. Fusarium solani pisi cutinase. Biochimie 82, 1015–1021 (2000).
29. Chen, S., Su, L., Chen, J. & Wu, J. Cutinase: Characteristics, preparation, and application. Biotechnol. Adv. 31, 1754–1767 (2013).
30. Nyyssölä, A. Which properties of cutinases are important for applications?. Appl. Microbiol. Biotechnol. 99, 4931–4942 (2015).
31. Wolfe, B. E. & Dutton, R. J. Fermented foods as experimentally tractable microbial ecosystems. Cell 161, 49–55 (2015).
32. Kellogg, E.E. Recipes for liquid yeast. In: Kellogg, E.E. Every-Day Dishes and Every-Day Work. Modern Medicine Publishing
Company: 1896, pp 38–39.
33. Slepecky, R. A. & Starmer, W. T. Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia
101, 823–832 (2009).
34. Varela, C. & Borneman, A. R. Yeasts found in vineyards and wineries. Yeast 34, 111–128 (2017).
35. Bozoudi, D. & Tsaltas, D. The multiple and versatile roles of Aureobasidium pullulans in the vitivinicultural sector. Fermentation
4, 85 (2018).
36. Wirth, F. & Goldani, L. Z. Epidemiology of Rhodotorula: An emerging pathogen. Interdiscip. Perspect. Infect. Dis. 2012, 465717
(2012).
37. Martin, V., Valera, M. J., Medina, K., Boido, E. & Carrau, F. Oenological impact of the Hanseniaspora/Kloeckera yeast genus on
wines—A review. Fermentation 4, 76 (2018).
38. Sun, P.-F. et al. Intraspecific variation in plant growth-promoting traits of Aureobasidium pullulans. Chiang Mai J. Sci. 46, 15–31
(2019).
39. Masaki, K., Kamini, N. R., Ikeda, H. & Iefuji, H. Cutinase-like enzyme from the yeast Cryptococcus sp. strain S-2 hydrolyzes
polylactic acid and other biodegradable plastics. Appl. Environ. Microbiol. 71, 7548–7550 (2005).
40. Murphy, C. A., Cameron, J. A., Huang, S. J. & Vinopal, R. T. Fusarium polycaprolactone depolymerase is cutinase. Appl. Environ.
Microbiol. 62, 456–460 (1996).
41. Bischoff, F., Litwińska, K. & Cordes, A. Three new cutinases from the yeast Arxula adeninivorans that are suitable for biotechnological applications. Appl. Environ. Microbiol. 81, 5497–5510 (2015).
42. Gostinčar, C. et al. Genome sequencing of four Aureobasidium pullulans varieties: Biotechnological potential, stress tolerance, and
description of new species. BMC Genom. 15, 549 (2014).
43. Kodama, Y. et al. Crystal structure and enhanced activity of a cutinase-like enzyme from Cryptococcus sp. strain S-2. Proteins 77,
710–717 (2009).
44. Soliday, C. L., Dickman, M. B. & Kolattukudy, P. E. Structure of the cutinase gene and detection of promoter activity in the 5’-flanking region by fungal transformation. J. Bacteriol. 171, 1942–1951 (1989).
45. Ohnishi, K., Toida, J., Nakazawa, H. & Sekiguchi, J. Genome structure and nucleotide sequence of a lipolytic enzyme gene of
Aspergillus oryzae. FEMS Microbiol. Lett. 126, 145–150 (1995).
46. van der Vlugt-Bergmans, C. J., Wagemakers, C. A. & van Kan, J. A. Cloning and expression of the cutinase A gene of Botrytis
cinerea. Mol. Plant Microb. Interact. 10, 21–29 (1997).
47. Sniegowski, P. D., Dombrowski, P. G. & Fingerman, E. Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural
woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast
Res. 1, 299–306 (2002).
48. Fay, J. C. & Benavides, J. A. Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet. 1, 66–71
(2005).
49. Duan, S.-F. et al. The origin and adaptive evolution of domesticated populations of yeast from Far East Asia. Nat. Commun. 9, 2690
(2018).
50. Gognies, S., Gainvors, A., Aigle, M. & Belarbi, A. Cloning, sequence analysis and overexpression of a Saccharomyces cerevisiae
endopolygalacturonase-encoding gene (PGL1). Yeast 15, 11–22 (1999).
51. Radoi, F., Kishida, M. & Kawasaki, H. Endo-polygalacturonase in Saccharomyces wine yeasts: Effect of carbon source on enzyme
production. FEMS Yeast Res. 5, 663–668 (2005).
52. Sugiura, H. et al. Bacterial inducible expression of plant cell wall-binding protein YesO through conflict between Glycine max and
saprophytic Bacillus subtilis. Sci. Rep. 10, 18691 (2020).
53. Armijo, G. et al. Grapevine pathogenic microorganisms: Understanding infection strategies and host response rcenarios. Front.
Plant Sci. 7, 382 (2016).
54. Kolattukudy, P. E. Biopolyester membranes of plants: Cutin and suberin. Science 208, 990–1000 (1980).
55. Miura, Y. The biological significance of ω-oxidation of fatty acids. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 89, 370–382 (2013).
56. Wertz, P. W. Naturally occurring ω-hydroxyacids. Int. J. Cosmet. Sci. 40, 31–33 (2018).
57. Toju, H., Tanabe, A. S., Yamamoto, S. & Sato, H. High-coverage ITS primers for the DNA-based identification of ascomycetes and
basidiomycetes in environmental samples. PLoS ONE 7, e40863 (2012).
58. Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37,
852–857 (2019).
59. Kántor, A., Mareček, J., Ivanišová, E., Terentjeva, M. & Kačániová, M. Microorganisms of grape berries. Proc. Latv. Acad. Sci. B
51, 502–508 (2017).
60. White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics.
In PCR Protocols: A Guide to Methods and Applications (eds Innis, M. A. et al.) 315–322 (Academic Press, 1990).
61. Nakagawa, T. et al. Peroxisomal membrane protein Pmp47 is essential in the metabolism of middle-chain fatty acid in yeast peroxisomes and is associated with peroxisome proliferation. J Biol Chem 275, 3455–3461 (2000).
62. Chen, S. et al. Identification and characterization of bacterial cutinase. J Biol Chem 283, 25854–25862 (2008).
Acknowledgements
This work was partly supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (grant numbers 20K05958 and 22H04885 to D.W.). The authors thank Yukiko Sugimoto for the
technical assistance and Enago (https://www.enago.com) for the English language review.
Scientific Reports |
Vol:.(1234567890)
(2023) 13:9279 |
https://doi.org/10.1038/s41598-023-35734-z
12
www.nature.com/scientificreports/
Author contributions
W.H. designed the study. D.W. performed the experiments. D.W. and W.H. analyzed the data. D.W. and W.H.
wrote the manuscript.
Competing interests The authors declare no competing interests.
Additional information
Supplementary Information The online version contains supplementary material available at https://doi.org/
10.1038/s41598-023-35734-z.
Correspondence and requests for materials should be addressed to W.H.
Reprints and permissions information is available at www.nature.com/reprints.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional affiliations.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International
License, which permits use, sharing, adaptation, distribution and reproduction in any medium or
format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the
Creative Commons licence, and indicate if changes were made. The images or other third party material in this
article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the
material. If material is not included in the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from
the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
© The Author(s) 2023
Scientific Reports |
(2023) 13:9279 |
https://doi.org/10.1038/s41598-023-35734-z
13
Vol.:(0123456789)
...