Paula Silva
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By Francesca Barbero, Irene Stefanini, Beatrice Valentini

It is currently recognized that grapes in the vineyard host a broad range of yeast species1. Recent studies are consolidating the observation that such yeast community (the mycobiota) not only resides on grape skin, but also affects vine health, growth, and yield2 as well as the organoleptic characteristics of the final product3-5. Even if most of the procedures currently adopted in the vineyards and the cellar involve treatments with antifungals (e.g. copper sulfate and sulfites), the vineyard mycobiota can positively (e.g. Saccharomyces cerevisiae, Hanseniaspora uvarum, Lachancea thermotolerans) or negatively (e.g. Zygoascus hellenicus or Botrytis spp.) impact must fermentation. This relevant role of the vineyard mycobiota in winemaking is increasingly acknowledged to the point that the new term “microbial terroir” is getting a foothold3. According to some reports, the vineyard mycobiota composition is influenced by geo-climatic elements (e.g. solar radiation, latitude, longitude, and  elevation), and physicochemical properties (such as total sugars, polyphenol, total acid, and pH)6. Although these factors may contribute to selecting the yeast species and strains capable of surviving in the vineyard environment, we are still far from understanding the actual source of vineyard yeasts. It is currently recognized that forests host many species of yeasts, therefore they may be a natural reservoir of these microorganisms7. However, we are still missing a key step in the potential journey of yeasts throughout environments: since most yeasts are not airborne (hence cannot be transported to the vineyard by wind), how can they reach the grapes in the vineyard? Our previous studies have shown that social wasps (e.g., hornets and European paper wasps) can vector Saccharomyces cerevisiae8-9, one of the most important yeasts for winemaking. Despite several insects bearing various yeast species10, social wasps show multiple features making them very promising vectors for many yeasts inhabiting the vineyard and playing a relevant role in winemaking. Social wasps adults feed mainly on sugar sources (such as grapes); the highest number of individuals per nest is reached in Autumn, when the grapes in the vineyard are ripe and, besides providing an attractive source of food for the animal, also become heavily populated by yeast cells, possibly vectored by insects11; their buccal apparatus is sufficiently strong to allow them to break hard substrates, such as the skin of pristine grapes; they live and forage in miscellaneous environments, thus they could gather most of the existing yeast diversity8.

We hypothesized that yeasts found in the vineyard originate from forests surrounding the vineyard and reach the grapes thanks to social insects acting as vectors. We could test this hypothesis thanks to the support of the Fondazione CRT-Cassa di Risparmio di Torino (https://fondazionecrt.it/) and to the collaboration of enthusiastic and farsighted Piedmontese winemakers: Paolo Ghislandi (I Carpini Wines, https://icarpini.it/), Enrico Rivetto (Rivetto wines, https://www.rivetto.it/en/), and Andrea Tirelli (Tirelli wines, https://www.tirellivini.it/), and other relevant contributors (listed at the page https://cutt.ly/jMaqhwx). We analyzed and compared the yeast communities present in the gut of wasps caught in six organic or biodynamic vineyards close (<500 m) and far (>500 m) from wooded areas. The analysis, conducted over two vintages (2020 and 2021), confirmed the hypothesis and provided some fundamental insights into the natural flow of yeasts. The presence of woods in the vineyards’ proximity influences multiple aspects of yeast populations vectored by social insects.

The wasps caught in vineyards close to wooded areas carried more abundant and diverse yeast populations than insects caught in vineyards distant from woods. This observation can be ascribed to the fact that the variegate wasps’ foraging substrates present in woodlands, including flowers, soil, fruit, small animals, and decaying material, represent an ample and diverse source of natural yeasts for insects7. Wasps caught in vineyards both close and far from woods bore yeast species currently reaping great success among winemakers because of their fermentative potentials, such as Lachancea thermotolerans and Metschnikowia pulcherrima. However, the mycobiota of wasps caught in vineyards close to woods was characterized by yeast species known to contribute to grape must fermentation and lacking in the mycobiota of wasps caught from vineyards far from woods. For instance, Saccharomyces cerevisiae, the yeast mainly responsible for the alcoholic fermentation of the must, could be found only in wasps caught in vineyards close to woods. Conversely, the mycobiota of wasps caught in vineyards far from wooded areas encompassed some yeast species potentially perilous for human health or for wine production, such as Cryptococcus neoformans. Peculiarities of the mycobiota of wasps caught in vineyards close to woods were observed not only at the species but also at the strain level, with these yeast isolates being characterized by a high capability of metabolizing the sugars present in plants, and this in the wasp food most abundant in the forest. Considering that previous studies highlighted significant differentiation between the mycobiota of geographically distant vineyards12, it was surprising to observe that, in our study, the differences in abundance, biodiversity, and composition of yeast communities vectored by wasps were more significant between insects collected in vineyards close and far from woods than in distantly located vineyards.

Overall, these results provide fundamental insights into the ecology of the vineyard mycobiota, highlighting the need to maintain a vineyard-forest mosaic landscape. The presence of wooded areas appears to be a fundamental source of yeast diversity, which, once transported to the vineyard by vectors such as social wasps, can contribute to the wine production process. A more “biodiverse” community, in which various yeasts can contribute individually to the fermentation process, has the potential to provide a concert of metabolic functions giving the product organoleptic characteristics that can hardly be obtained by using the current oenological techniques based on the activity of one or a few fungal species.

 

For further details: https://www.frontiersin.org/articles/10.3389/fmicb.2022.1039939/full

 

Francesca Barbero is an Associate Professor of Zoology at the University of Turin (Italy), Department of Life Sciences and Systems Biology. She graduated in Biological Sciences and her Ph.D. in Evolutionary Biology and Biodiversity Conservation at the University of Turin.

The aspect that most characterizes her research is the study of communication and mimicry mechanisms implemented in host-parasite interactions and, more generally, in multitrophic systems that involve plants or microorganisms and insects. Another important area of research is the investigation of the biology, ecology, and conservation of diurnal Lepidoptera and Hymenoptera. She is Associate Editor for the journal Insect Conservation and Diversity, Topic Editor for the International Journal of Molecular Sciences, and manuscript manager for the Journal of Plant Interactions. She has led or participated in international, national, and local research projects in entomology and is also the PI for basic or applied research agreements with parks and private companies. She is an auditor for national (e.g., PRIN) and international projects. She is a member of UZI (Italian Zoological Union), SEL (Societas Europea Lepidopterologica), CSEE (Canadian Society for Ecology & Evolution), SIE (Società Italiana di Etologia), and a founding member of ALI (Italian Lepidopterological Association). She is also a certified specialist for BRC Global Standards – Food safety, as a counselor for pest control strategy in Food Factories. Her team lab now counts one senior researcher, one postdoc fellow, three Ph.D. students, and several Master and Bachelor students.

Irene Stefanini is a Senior Researcher at the University of Turin (Italy), Department of Life Sciences and Systems Biology. She got her Master’s degree in Industrial and Environmental Biotechnology at the University of Florence, where she also obtained her PhD in Pharmacology and Toxicology. After a three-year postdoctoral experience at the Fondazione Edmund Mach, in Trento (Italy), where she studied the dynamic of yeast communities in spontaneous grape must fermentations, she obtained a position as an Independent Research Fellow at the University of Warwick (UK), where she leads researches on the associations between yeast genomics and phenotypes. In 2019, she got back to Italy as a Researcher at the University of Turin, where continued her studies on yeast ecology and evolution. Her current interest is mostly focused on the dissection of the interactions between yeast and some of their host (primarily insects) and on the impact of these associations on anthropic activities and yeast ecology and evolution. She is a member of the Editorial Board of the Yeast journal (Wiley) and serves as a reviewer for several of the most renowned international journals in the field of microbiology. She has participated in international research projects in the field of microbiology and is currently leading international and local research projects also in collaboration with multidisciplinary and international research groups.

Beatrice Valentini is a PhD student in Sustainable Development and Cooperation at the University of Turin, Department of Life Sciences and Systems Biology, Italy. She got her Master’s degree in Pharmaceutical, Veterinary, and Medical Biotechnology, and, after a period spent working as a Biologist in a diagnostic laboratory, she returned to Academy at the University of Turin. She is currently working in the field of microbial ecology, mainly studying the links between the yeast populations inhabiting vineyards and the characteristics of the surrounding environmental matrix. Her PhD project focuses on the investigation of the factors of the environmental matrix or anthropic contributing to the definition of the microbial diversity present in the vineyard and hence potentially influencing the organoleptic characteristics of the wine. Thanks to her results, she aims to improve the sustainability of wine production and enhance the typicality of the product.

References

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