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Biodiversity of Oenological Lactic Acid Bacteria: Species- and Strain-Dependent Plus/Minus Effects on Wine Quality and Safety

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Biodiversity of Oenological Lactic Acid Bacteria: Species- and Strain-Dependent Plus/Minus Effects on Wine Quality and Safety fermentation Review Biodiversity of Oenological Lactic Acid Bacteria: Species- and Strain-Dependent Plus/Minus Effects on Wine Quality and Safety Vittorio Capozzi 1,† , Maria Tufariello 2,† , Nicola De Simone 3, Mariagiovanna Fragasso 3 and Francesco Grieco 2,* 1 National Research Council—Institute of Sciences of Food Production (ISPA) c/o CS-DAT, Via Michele Protano, 71121 Foggia, Italy; [email protected] 2 National Research Council—Institute of Sciences of Food Production (ISPA), Via Prov.le, Lecce-Monteroni, 73100 Lecce, Italy; [email protected] 3 Department of Agriculture, Food, Natural Resources, and Engineering, University of Foggia, 71121 Foggia, Italy; [email protected] (N.D.S.); [email protected] (M.F.) * Correspondence: [email protected]; Tel.: +39-0832422612 † These authors contributed equally to this work. Abstract: Winemaking depends on several elaborate biochemical processes that see as protagonist ei- ther yeasts or lactic acid bacteria (LAB) of oenological interest. In particular, LAB have a fundamental role in determining the quality chemical and aromatic properties of wine. They are essential not only for malic acid conversion, but also for producing several desired by-products due to their important enzymatic activities that can release volatile aromatic compounds during malolactic fermentation (e.g., esters, carbonyl compounds, thiols, monoterpenes). In addition, LAB in oenology can act as bioprotectors and reduce the content of undesired compounds. On the other hand, LAB can affect wine consumers’ health, as they can produce harmful compounds such as biogenic amines and ethyl carbamate under certain conditions during fermentation. Several of these positive and negative Citation: Capozzi, V.; Tufariello, M.; properties are species- and strain-dependent characteristics. This review focuses on these aspects, De Simone, N.; Fragasso, M.; Grieco, F. Biodiversity of Oenological summarising the current state of knowledge on LAB’s oenological diversity, and highlighting their Lactic Acid Bacteria: Species- and influence on the final product’s quality and safety. All our reported information is of high interest in Strain-Dependent Plus/Minus Effects searching new candidate strains to design starter cultures, microbial resources for traditional/typical on Wine Quality and Safety. products, and green solutions in winemaking. Due to the continuous interest in LAB as oenological Fermentation 2021, 7, 24. https:// bioresources, we also underline the importance of inoculation timing. The considerable variability doi.org/10.3390/fermentation7010024 among LAB species/strains associated with spontaneous consortia and the continuous advances in the characterisation of new species/strains of interest for applications in the wine sector suggest that Received: 30 December 2020 the exploitation of biodiversity belonging to this heterogeneous group of bacteria is still rising. Accepted: 12 February 2021 Published: 17 February 2021 Keywords: malolactic fermentation; lactic acid bacteria; malolactic bacteria; Oenococcus oeni; Lactiplantibacillus plantarum; wine; aroma; biogenic amines; lactobacilli; biocontrol Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. LAB in Oenology: Introductory Aspects and Biodiversity During the winemaking process, lactic acid bacteria (LAB) promote the decarboxyla- tion of L-malic acid to L-lactic acid, which is denoted as malolactic fermentation (MLF) [1]. This biological process occurs at the end of the alcoholic fermentation (AF), the principal Copyright: © 2021 by the authors. Saccharomyces Licensee MDPI, Basel, Switzerland. phase in winemaking, which is conducted by yeasts (mainly belonging to the This article is an open access article genus, but together, in some cases, with selected non-Saccharomyces strains) [2–4]. MLF is distributed under the terms and required for aged red wines and some young red, white, and base sparkling wines, since conditions of the Creative Commons it supplies microbiological stabilisation by reducing the nutrients in wine and lowers the Attribution (CC BY) license (https:// acidity of the final product [5,6]. Specific management of microbial resources inoculated to creativecommons.org/licenses/by/ promote desired biochemisms (e.g., co-inoculation), can favour a simultaneous progression 4.0/). of AF and MLF [7,8]. Fermentation 2021, 7, 24. https://doi.org/10.3390/fermentation7010024 https://www.mdpi.com/journal/fermentation Fermentation 2021, 7, 24 2 of 17 MLF enhances wine flavour and aroma complexity by freeing relevant amounts of carbonyl compounds, such as diacetyl (2,3-butanedione), which contributes to a wine’s buttery flavour [9]. Moreover, LAB species have demonstrated an ability to promote several biochemical modifications of wine able to enhance its aroma, such as the release of volatile thiols from precursor compounds, methionine metabolism, glycosidases, and esterase activities [10–12]. However, during winemaking, the MLF dynamics are often unpredictable, and it is problematic to monitor or manage. Spontaneous MLF may affect wine quality, since the production of bacteria-derived off-flavour molecules (such as volatile phenols and acetic acid) and compounds dangerous to consumer health, i.e., biogenic amines (BAs) and ethyl carbamate. Thus, it is necessary to exert the microbiological control of this biochemical process throughout the winemaking process to guarantee the final product’s quality and safety [13]. A composite microbial consortium is implicated in the winemaking process, comprising yeast, bacteria, fungi, and viruses [14–16]. Concerning LAB, they are indeed present on both grape skins and cellar environment equipment [17], but the operators can directly inoculate them by the addition of selected starter cultures [18]. LAB, microaerophiles, and Gram-positive bacteria specifically produce lactic acid as a primary metabolite of glucose catabolism [19]. Consistent with their glucose catabolic activity, they can be distributed into two groups: bacteria that ferment glucose with lactic acid as the main by-product (homofermentative), and the others that produce ethanol, carbon dioxide, and lactic and acetic acid after glucose fermentation (heterofermentative). The most common LAB isolated from musts and wine are oenoccocci, lactobacilli and pediococci (Table1). Table 1. Species of selected lactic acid bacteria found in association with raw materials in representative phases of winemaking (grape harvest, must alcoholic fermentation, wine malolactic fermentation), according to selected studies [20–25]. Grape and Harvest Must and AF Wine and MLF Oenococcus oeni (80–100%) Lactiplantibacillus plantarum Lentilactobacillus hilgardii Lentilactobacillus buchneri Oenococcus oeni (0–10%) Lentilactobacillus diolivorans Limosilactobacillus alvi Lacticaseibacillus casei Levilactobacillus brevis Latilactobacillus curvatus Limosilactobacillus frumenti Limosilactobacillus alvi Liquorilactobacillus mali Levilactobacillus brevis Apilactobacillus kunkeei Oenococcus oeni Limosilactobacillus frumenti Fructilactobacillus lindneri Lactiplantibacillus plantarum Secundilactobacillus collinoides Fructilactobacillus sanfranciscensis Lentilactobacillus hilgardii Lacticaseibacillus paracasei Lentilactobacillus kefiri Levilactobacillus brevis Lactiplantibacillus pentosus Lactococcus lactis Fructilactobacillus lindneri Liquorilactobacillus mali Enterococcus faecium Limosilactobacillus frumenti Fructilactobacillus lindneri Enterococcus avium Lactococcus sp. Fructilactobacillus fructivorans Enterococcus durans Pediococcus parvalus Lactobacillus delbrueckii Enterococcus hermanniensis Lactococcus lactis Leuconostoc mesenteroides Leuconostoc citreum Pediococcus damnosus Leuconostoc fructosum Pediococcus parvalus Leuconostoc mesenteroides Weissella paramesenteroides Enterococcus faecium Pediococcus damnosus Pediococcus parvalus Weissella paramesenteroides Note: AF, alcoholic fermentation; MLF, malolactic fermentation. The O. oeni species has ellipsoidal-to-spherical cells typically present in pairs or short chains. It is an asporogenous and nonmotile bacteria with an optimal growth range between pH 4.8–5.5 and 20–30 ◦C. The O. oeni population typically raises during the AF, and it often becomes the only species found in wine at the end of MLF [26,27]. O. oeni is the principal Fermentation 2021, 7, x FOR PEER REVIEW 3 of 21 Fructilactobacillus sanfrancis- Levilactobacillus brevis censis Limosilactobacillus frumenti Lentilactobacillus kefiri Secundilactobacillus collinoides Lactococcus lactis Lacticaseibacillus paracasei Enterococcus faecium Lactiplantibacillus pentosus Enterococcus avium Liquorilactobacillus mali Enterococcus durans Fructilactobacillus lindneri Enterococcus hermanniensis Fructilactobacillus fructivorans Leuconostoc mesenteroides Lactobacillus delbrueckii Pediococcus damnosus Lactococcus lactis Pediococcus parvalus Leuconostoc citreum Weissella paramesenteroides Leuconostoc fructosum Leuconostoc mesenteroides Enterococcus faecium Pediococcus damnosus Pediococcus parvalus Weissella paramesenteroides Note: AF, alcoholic fermentation; MLF, malolactic fermentation. The O. oeni species has ellipsoidal-to-spherical cells typically pre- sent in pairs or short chains. It is an asporogenous and nonmotile bac- teria with an optimal growth range between pH 4.8–5.5 and 20–30 °C. Fermentation 2021, 7, 24 The O. oeni population typically raises during
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