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García-Izquierdo, I.; Colino-Rabanal, V.J.; Tamame, M.; Rodríguez-López, F. Ecosystem-Services Provided by Microbiota in Vineyards and Wines. Encyclopedia. Available online: https://encyclopedia.pub/entry/53571 (accessed on 18 June 2024).
García-Izquierdo I, Colino-Rabanal VJ, Tamame M, Rodríguez-López F. Ecosystem-Services Provided by Microbiota in Vineyards and Wines. Encyclopedia. Available at: https://encyclopedia.pub/entry/53571. Accessed June 18, 2024.
García-Izquierdo, Isabel, Victor J. Colino-Rabanal, Mercedes Tamame, Fernando Rodríguez-López. "Ecosystem-Services Provided by Microbiota in Vineyards and Wines" Encyclopedia, https://encyclopedia.pub/entry/53571 (accessed June 18, 2024).
García-Izquierdo, I., Colino-Rabanal, V.J., Tamame, M., & Rodríguez-López, F. (2024, January 08). Ecosystem-Services Provided by Microbiota in Vineyards and Wines. In Encyclopedia. https://encyclopedia.pub/entry/53571
García-Izquierdo, Isabel, et al. "Ecosystem-Services Provided by Microbiota in Vineyards and Wines." Encyclopedia. Web. 08 January, 2024.
Ecosystem-Services Provided by Microbiota in Vineyards and Wines
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The progression in next-generation sequencing (NGS) technologies is helping to facilitate the identification of microbial dynamics during winemaking. These advancements have aided winemakers in gaining a more comprehensive understanding of the role of microbiota in the fermentation process, which, in turn, is ultimately responsible for the delivery of provisioning (wine features and its production), regulating (such as carbon storage by vineyards, regulation of soil quality, and biocontrol of pests and diseases) or cultural (such as aesthetic values of vineyard landscapes, scholarly enjoyment of wine, and a sense of belonging in wine-growing regions) ecosystem services. Ecosystem services can be defined as the conditions and processes through which natural ecosystems and their component species sustain and enable human life. The main classifications group them into three broad categories: provisioning, regulating, and cultural.

ecosystem services microbiota vineyard wine carbon storage soil quality biological control culture

1. Introduction

The human transformation of nature on a global scale, especially in recent decades, has led to a marked decline in indicators related to ecosystem health and biodiversity [1] and, with it, a decline in the benefits that all humans derive from ecosystem services. Ecosystem services can be defined as the conditions and processes through which natural ecosystems and their component species sustain and enable human life [2][3]. The main classifications group them into three broad categories: provisioning, regulating, and cultural [4][5]. The ecosystem services concept is the main tool used for calculating the value of natural capital [6].
Minimising the negative consequences of human transformations on the environment requires that each production sector adopts practices to reduce (or even neutralise) its net impact on ecosystems and biodiversity, while keeping (or even increasing) the flow of benefits that we obtain from nature. One of the production sectors with the greatest impact is agriculture, which is required to meet the food demands of the growing world population [7][8]. In fact, one of the main challenges for agriculture in the 21st century is the generation of multifunctional landscapes in which food is produced (provisioning service) at the same time as it promotes the supply of many other regulating and cultural services [9][10].
The wine sector is no stranger to this goal. Currently, vineyards occupy 7.3 million hectares worldwide, producing up to 260 million hectolitres to satisfy an estimated world consumption of 236 million hectolitres [11]. Efforts are being made in different wine regions in the form of pilot projects to integrate ecosystem services, biodiversity, and multifunctionality as relevant elements in vineyard management decision making [12][13][14][15][16][17]. Nevertheless, despite being a provider of relevant ecosystem services, the role of microbiota is commonly ignored in most approaches [18].
Microbiota provide ecosystem services both for vineyards and for the quality of the final product, wine. This research uses the classification proposed by the United Nations System of Environmental-Economic Accounting, which identifies three main groups: provisioning, regulating, and cultural ecosystem services [5].

2. Provisioning Ecosystem Services

Within the category of provisioning ecosystem services, microbiota are closely linked to wine production through fermentation. They also provide remarkable genetic diversity that can benefit the wine industry and wine cultures.

2.1. Biomass (Crop) Provisioning Services

Without microbiota, humans would simply not have wine. It plays a fundamental role in fermentation, transforming grape must into wine. Thanks to studies based on HTS, the existence of a large microbial pool that includes fungi and bacteria in spontaneous wine fermentation has been proven [19][20][21][22]. The different strains of oenological yeast have been “domesticated” over the years, adapting by evolutionary mechanisms to environments with many stress factors in the fermentation process [23][24][25]. Thus, regarding alcoholic fermentation, indigenous species of the genera Hanseniaspora, Candida, Pichia, and Metschnikowia are involved in the first steps of the process, producing secondary metabolites (such as acids, alcohols, and esters) and enzymes (such as esterases, lipases, and proteases) that can affect the final quality of the wine [26]. These species can grow at low ethanol concentrations, but when this exceeds 5–7% and the abundance of fermented sugars begins to decrease, they start to decline and die [27]. Other yeasts, such as species of Brettanomyces, Kluyveromyces, Schizosaccharomyces, Torulaspora, and Zygosaccharomyces, may also be present during fermentation and subsequently in wine, some of which are capable of adversely affecting sensory quality [23]. Due to its high fermentation capacity, ethanol tolerance, and strong resistance to the toxicity of different metabolites, S. cerevisiae prevails in the final stages of fermentation [28][29], being nearly unique in those fermentations with commercial starters, or else, accompanied by other species, such as Torulaspora delbrueckii, Zygosaccharomyces fermentati, Kluyveromyces thermotolerans, Hanseniaspora guilliermondii, and Dekkera anomala in spontaneous fermentation [26][30][31]. For malolactic fermentation, Oenococcus oeni is the dominant species [32][33][34]. Apart from the gradual growth of different yeast species during fermentation, the existence of the underlying successional development of different strains within each species has also been described [27].
Microbiota play a remarkable role in the organoleptic characteristics of wine. For example, beneficial yeast species of Debaryomyces may produce enzymes, such as β-glucosidases, which increase the concentration of desirable organoleptic compounds in wines [35]. Lachancea thermotolerans, Pichia kluyveri, Rhodotorula mucilaginosa, and Metschnikowia spp. may improve the flavour and aroma of wine [29][36][37][38]. Species of bacteria, such as those included in the genus Lactobacillus, contribute to the synthesis of methyl and isobutyl esters and the formation of red and black fruity wine fragrances. Fructobacillus is closely related to the synthesis of aromatic alcohols and the generation of fruity flavours [39].
In spontaneous fermentation, the soil microorganisms that are present in grape berry and those present only in berries (coming from insects, birds, etc.) produce wines with greater complexity than those fermented with pure starters, providing a bouquet of flavours perceived as more attractive to consumers [40][41][42][43]. These spontaneously fermented wines are practically impossible to reproduce in later vintages or in some regions, mainly due to terroir differences [44][45]. However, these wines are unpredictable due to fermentation arrests and can deteriorate due to the appearance of certain undesirable yeast species, such as Brettanomyces spp. [46].

2.2. Genetic Material Services

The oenological microbiota constitutes a reservoir of great genetic diversity, with a wide variety of Saccharomyces and non-Saccharomyces yeast species and strains, which stems from mechanisms such as heterozygosity, nucleotide and structural variations, horizontal gene transfer, and intraspecific hybridisation [47][48]. This genetic diversity is likely to provide resilience to climate change in wine production [19][22][49] and can be exploited to obtain higher quality wines [50][51][52] or to generate non-GMO hybrids to be used as commercial starters that do not suppress the native microbial flora [53]. The species most sought after are those that ferment well and produce less ethanol, more glycerol, and more attractive aroma compounds. Some of these yeasts are non-Saccharomyces, such as Hanseniaspora vineae and Metschnikowia fructicola [53], or other species of Saccharomyces belonging to the sensu stricto complex [54][55], such as S. kudriavzevii, which can produce more aroma compounds and even higher amounts of other alcohols, such as phenylethanol. Saccharomyces uvarum also produces more aromatic compounds, such as alcohols and esters. Saccharomyces bayanus is cryotolerant, allowing for fermentation at lower temperatures [56][57][58][59][60][61]. In addition, the sequential fermentation of S. cerevisiae with non-Saccharomyces yeasts, such as Meyerozyma guilliermondii and Hanseniaspora uvarum, enhances floral and fruity aromas in wines [51].

3. Regulating Ecosystem Services

The interactions between biological communities (including microbiota) and the physical and chemical properties of the soil environment are fundamental to the processes, functions, and ecosystem services provided by nature in vineyards, such as carbon storage [62], regulation of soil quality [63], formation of soil structure [64], or the biocontrol of pests and diseases [62][65][66].

3.1. Carbon Storage

As vineyards are a potential source of carbon storage [67], with differences among vine ages [68] and grape varieties [69], soil microorganisms are of great importance in regulating organic carbon dynamics [70], as taxa such as Patescibacteria, Synergistetes, Chloroflexi, Actinobacteria, Deinococcus-Thermus, and Atribacteria can degrade organic carbon to produce organic acids [71].

3.2. Soil Quality Regulation Services

Microbial communities play a pivotal role in shaping soil nutrient dynamics, and any shift in their activities and functions has the potential to jeopardise soil biogeochemical cycles, ultimately impacting the availability of nutrients to plants [62][72][73][74]. Thus, there are specific microbial consortia that lead to nitrogen fixation and nutrient mineralisation, metabolising, for example, recalcitrant forms of N, K, and P to release these essential elements for vine nutrition [75][76][77].

3.3. Soil and Sediment Retention Services

Given the characteristics of the crop, its management, and its location in topographically complex areas, vineyards present a particularly favourable context for soil loss compared to other agricultural land [78][79]. The microbiome can contribute to reducing this problem. In this regard, the arbuscular mycorrhizal fungi (AMF) of the subphylum Glomeromycotina promote the formation of soil aggregates and thus the prevention of soil erosion [80][81][82][83][84]. AMF develops a dense mycelial network in the soil [85][86], which, together with the secretion of sticky substances comprised of proteins [87], can have a binding action on soil particles and improve their structure, leading to increased structural stability and soil quality [88][89][90]. Thus, a reduction in AFM is expected to increase the risk of erosion [91].

3.4. Biological Control Services

Understanding the microbial ecology of vineyards has implications for disease management and the development of more sustainable and eco-friendly approaches to protecting grapevines. Bacteria present in the rhizosphere and endosphere of vine shoots and branches, such as Achromobacter xylosoxidans, Bacillus subtilis, and Pseudomonas fluorescens, can produce siderophores that limit the availability of iron, thus reducing the presence of pathogenic microorganisms. Some bacteria also degrade virulence factors (e.g., oxalic acid) produced by plant pathogens, thus reducing the severity of damage [92]. By making good use of the functionalities provided by the microbiome, chemical products are starting to be replaced by selected bacterial strains, endophytic fungi, and yeasts that show defensive responses to grapevine pathogens [93], such as powdery mildew (Uncinula necator), downy mildew (Plasmopara viticola), or Botrytis cinerea, which can negatively affect the quality of the final product [94][95]. This biocontrol is provided by species such as Lysobacter capsici (AZ78), Trichoderma spp. [96][97][98][99][100], and Aureobasidium pullulans [101][102][103]. The use of these microorganisms instead of chemical fungicides helps in the production of certified organic wines [104][105]. Biological control of microorganisms is an active field of research in which significant progress is being made. For instance, strains of Arthrobacter spp., Rhodococcus spp., and Bacillus mycoides with an excellent ability to reduce the growth of mycotoxins from the fungi Aspergillus carbonarius, A. niger, and A. flavus have recently been isolated from organic vineyard soils [106]. In addition, some yeasts derived from grape must are also effective against pathogens such as B. cinerea [107], making them potential candidates for industrial application as biological control agents.

3.5. Nursery Population and Habitat Maintenance Services

Microbiota can provide better soil conditions for vine development. For example, the fungus Aerobasidium pullulans is known to metabolise inorganic sulphur used as a fertiliser and pesticide and to absorb copper employed as a fungicide, which in high concentrations is toxic to the plant [101][102].

4. Cultural Ecosystem Services

Beyond the provisioning services, an ancestral culture has been created around wine, expressed in a rich tangible and intangible heritage that is ultimately based on the fermentation process carried out by the microbiota. These cultural services are expressed in the form of enotourism, the aesthetic values of vineyard landscapes, the scientific development of oenology, the scholarly enjoyment of wine, the identity and sense of belonging in wine-growing regions, symbolism, and even certain spiritual values [15][62][108].

4.1. Recreation-Related Services

Enotourism includes all tourist activities related to the world of wine: wine tasting, visits to vineyards and wineries in different wine-growing regions, festivals, and other organised wine-related events [109]. The differences between wine production terroirs are what give “typicity” and “identity” to the wine produced in different territories and, ultimately, a “sense of place” to the communities linked to its production.

4.2. Visual Amenity Services

The beauty of the landscape increases the market value of wine-related products [15][108][110]. Given that humans aesthetically prefer healthy plants and that the fungal and bacterial diversity of leaves is closely related to the health status of grapevines [111], the microbiota is also related to the visual appreciation of vineyard landscapes.

4.3. Education, Scientific, and Research Services

The diversity provided by the different terroirs encourages scientific research in the field of oenological microbiology, aimed at unravelling the interactions between the microbiota, the vine, and the final product [62][112].

4.4. Spiritual, Artistic, and Symbolic Services

Wine has been linked to various myths, rites, and religious cults for thousands of years [113][114][115][116]. The Greek god Dionysus, reinterpreted as Bacchus in Roman mythology, was the revealer of wine culture. Among Egyptian deities, Hathor, the goddess of wine, was carved into the amphorae used to store it, while Osiris gave the people instructions on how to harvest the vine and store the wine. The Sumerians incorporated the goddess Geshtinanna, a name that means “mother vine”, as found in various inscriptions.

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