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Article

Interactions among Relevant Non-Saccharomyces, Saccharomyces, and Lactic Acid Bacteria Species of the Wine Microbial Consortium: Towards Advances in Antagonistic Phenomena and Biocontrol Potential

by
Marianna De Gioia
1,
Pasquale Russo
2,
Nicola De Simone
1,
Francesco Grieco
3,*,
Giuseppe Spano
1,
Vittorio Capozzi
4 and
Mariagiovanna Fragasso
1,*
1
Department of Agriculture Food Natural Science Engineering, University of Foggia, Via Napoli 25, 71122 Foggia, Italy
2
Department of Food, Environmental and Nutritional Sciences, University of Milan, Via Luigi Mangiagalli 25, 20133 Milano, Italy
3
Institute of Sciences of Food Production, National Research Council, Via Prov.le, Lecce-Monteroni, 73100 Lecce, Italy
4
Institute of Sciences of Food Production, National Research Council (CNR), c/o CS-DAT, Via Michele Protano, 71121 Foggia, Italy
*
Authors to whom correspondence should be addressed.
Appl. Sci. 2022, 12(24), 12760; https://doi.org/10.3390/app122412760
Submission received: 16 November 2022 / Revised: 1 December 2022 / Accepted: 9 December 2022 / Published: 12 December 2022
(This article belongs to the Special Issue New Frontiers in Wine Sciences)
Browse Figure
Versions Notes

Abstract

:
The topic of microbial interactions is of notable relevance in oenology, being connected with their impact on microbial biodiversity and wine quality. The interactions among different couples of microorganisms, in particular yeasts and lactic acid bacteria representative of the must/wine microbial consortium, have been tested in this study. This interaction’s screening has been implemented by means of plate assays, using culture medium, grape juice, and wine agar as substrates. Different antagonistic phenomena have been detected, belonging to the following interaction categories: yeast-yeast, yeast-bacteria, bacteria-yeast, and bacteria-bacteria. In general, the inhibitory activity has been observed in all three media agar used as substrates, resulting in more frequent on culture medium, followed by grape juice and, finally, wine. Specifically, the work is one of the first reports demonstrating the reciprocal interactions between non-Saccharomyces yeasts (NSY) and malolactic bacteria. The findings shed new light on the co-inoculation of the yeast starter culture with malolactic bacteria, as well as the biocontrol potential of Lactic Acid Bacteria (LAB) strains. Highlighted microbial interactions are relevant for the management of alcoholic fermentation, malolactic fermentation, and the development of distinctive aroma profiles, control of spoilage yeasts, and the selection of tailored mixed starter cultures. In addition, the plate assay method could be a fast, cheap, and suitable method to exclude negative interactions among Saccharomyces spp., NSY, and malolactic bacteria during trials from regional spontaneous fermentations with the aim to select tailored mixed starter cultures.

1. Introduction

As reviewed by Liu et al. [1] the Wine Microbial Consortium (WMC) is mainly composed of different microorganisms belonging to Saccharomyces spp., Non-Saccharomyces Yeasts (NSY), Lactic Acid Bacteria (LAB) Species, Acetic Acid Bacteria (AAB) species, Bacillus spp., and filamentous fungi, all microbes with diverse origins, occurrences, and paths of diffusion from the field to the winery [2]. In particular, Saccharomyces spp., NSY, and LAB are considered pro-technological microbes in oenology and play a pivotal role in the production of high-quality wines [3]. To a different extent, microbial diversity within these three classes contributes to shaping sensory characteristics and the safety of wine [4,5]. In fact, Saccharomyces spp., NSY, and LAB are present in spontaneous wine microbial consortia and used as starter cultures in oenology [6,7]. Saccharomyces spp. play the key role in Alcoholic Fermentation (AF), determining wine production and shaping wine quality crucially [8,9]. The positive effect of non-Saccharomyces yeasts can be dual. On the one side, NSY can be relevant for specific pro-technological applications [10,11,12,13,14]. On the other, they produce a variety of volatile compounds and extracellular enzymes with an important impact on the sensorial profile of wine [15,16]. These yeasts prevail at the beginning of the vinification process and are quickly replaced by S. cerevisiae, which completes AF, in reason of the different tolerance to peculiar wine stressors, such as ethanol and SO2. Concerning the role of LAB in the microbial wine-associated ecosystem, specific malolactic bacteria concerns modulate both microbial stability and sensorial quality of wine [17,18]. They consume residual nutrients and synthesize inhibitory compounds, contrasting the growth of undesired microbes [19]. LAB can produce volatile secondary metabolites with a positive impact on wine’s chemical composition and aroma [4,20].
Irrelevant, positive, and negative interactions can influence the growth and/or the metabolic activity of the species composing the WMC, affecting the evolution of microbial resources during fermentation and wine quality [1,21]. The WMC interactions include direct (cell-cell contact, quorum sensing, predation, parasitism, symbiosis, and inhibition) and indirect (neutralism, mutualism, commensalism, amensalism, and competition) interactions [22]. Several studies delve into the principal interactions among the main categories belonging to the wine microbial consortium: yeast-yeast (Saccharomyces spp.-Saccharomyces spp. [22,23]; Saccharomyces spp.-NSY [24,25]; NSY-NSY [26,27]), yeast-bacteria (NSY-LAB [28,29,30]; Saccharomyces spp.-LAB [31]), bacteria-yeast (LAB-NSY [32,33]; LAB-Saccharomyces spp. [34]), bacteria-bacteria (LAB-LAB [35]).
The heterogeneity, oenological significance, and the temporary succession of the different microbial categories contribute to must/wine microbiota, making this system an interesting model to study microbial interactions. In the last years, different methods and substrates have been used to test the relationships among microorganisms of enological interest. Generally, their evaluation is performed on plates [36,37,38], through co-/sequential inoculation in culture medium [39,40], synthetic [41], and commercial [36,42,43] grape juice/must or wine. In this context, the present work aims to verify, using an integrated plate assays methodological approach, the occurrence and the extent of interactions among all the possible combinations of non-Saccharomyces, Saccharomyces, and lactic acid bacteria isolated from spontaneous fermentations, used as oenological starter cultures, or from public collections. Interactions among yeasts and bacteria affect the wine quality, but only limited information on these phenomena is reported in the scientific literature [44]. Here, plate assays have been selected as a low-cost and fast method to evaluate the interactions for a large number of strains, with the novelty of introducing the use of plates made by including must and wine in order to achieve, despite the limitations of plate screening, a progressive approach with respect to oenological conditions.

2. Materials and Methods

2.1. Microorganisms

Forty-five microbial strains belonging to 15 different species of enological interest have been used in this work (Table 1).
In particular, bacterial species included three strains of Oenococcus oeni, 5 Lactiplantibacillus plantarum strains, one Pediococcus spp., and one strain for each of the following species: Levilactobacillus brevis, Pediococcus parvulus, Lentilactobacillus hilgardii. The yeast species included Saccharomyces cerevisiae (7 strains), Torulaspora delbrueckii (3 strains), Hanseniaspora uvarum (2 strains), Metschnikowia pulcherrima (10 strains), Pichia fermentans (3 strains), Brettanomyces bruxellensis (5 strains), Hanseniaspora guillermondii (1 strain), Issatchenkia terricola (1 strain), and Starmerella bacillaris (1 strain). The microorganisms submitted to this analysis derived from public collections, isolated from wine commercial starter cultures, or they have been isolated from spontaneous oenological fermentations (e.g., [42,45,46,47,48,49,50,51]) (Table 1). All the microbial strains have been stored at −80 °C in MRS or YPD medium and added with 30% of glycerol for bacteria and yeasts, respectively.

2.2. Culture Medium and Growth Conditions

Yeast cultures were grown in YPD broth: 10 g/L of yeast extract (Oxoid, Basingstoke, UK), 20 g/L of bacteriological peptone (Oxoid), and 20 g/L of dextrose (Oxoid). The growth of non-Saccharomyces yeasts was also evaluated in WL nutrient broth (Wallerstein Laboratory, Oxoid) [52]. Malolactic bacteria were grown in MRS broth (Oxoid), or MRS supplemented with 10 g/L of L-malic acid (Sigma Aldrich, St Louis, MO, USA) and adjusted to pH 5.5, with 1 M NaOH (Sigma Aldrich), for O. oeni strains. The growth of all microorganisms was carried out at 30 °C for 48 h, apart from O. oeni strains that were incubated in a jar (anaerobic conditions) for a week.
Considering the media for the plate screening, for yeast-yeast interactions YPD medium has been used for both layers; for bacteria-bacteria interactions, MRS medium has been employed for both layers; while, for bacteria-yeast and yeast-bacteria interactions, MRS and YPD media have been used for the bottom and/or top layer, respectively. The concentration of microbial suspensions was assessed by spectrophotometric (turbidimetric) analysis.

2.3. Interaction Plate Screening: Double-Layer Agar Diffusion Assay

The interactions between couples of microorganisms have been evaluated using (i) YPD and MRS culture medium, (ii) commercial red grape juice (VitaFit; Emig GmbH, Rellingen, Germany), and (iii) commercial red and white wine (alcohol concentration 10.5% (w/v); pH 3.5) as substrate.
The first methodological approach to test microbial interactions has been a double-layer agar diffusion assay, proposed by Comitini et al. [53]. A layer of culture medium agar (10 mL) was poured into Petri dishes. After solidification, 5 µL of six different strains overnight cultures were seeded to form rings of inoculum.
Plates have been incubated at room temperature (25–30 °C) for 24 h or, in the case of O. oeni strains, in the jar for a week. After that time, a top layer of culture medium soft agar (10 mL; 1% of agar), containing 6·× 105 CFU/mL of another strain, was poured onto the bottom layer and, finally, the Petri dishes incubated for about 72 h at room temperature.

2.4. Interaction Plate Screening: Agar Diffusion Assay

To simulate the real situation, the evolution of must/wine microbial consortium and the interactions between microorganisms have been tested in grape juice and wine. This attempt has been implemented through agar diffusion assay. This method has been suggested by Mehlomakulu et al. [38] and, unlike the above-described approach, was performed on a single layer. Grape juice has been added with 1% of yeast extract only to test the interactions involving bacteria (to “simulate” the conditions occurring at the end of AF) and adjusted to pH 4.5 with 1 M NaOH; this medium has been heated up to reach 55 °C and kept at this temperature. 1:100 v/v of each strain overnight culture have been inoculated into 7.5 mL of the modified grape juice. Hence, 2.5 mL of 4% agar (kept at 55 °C) was mixed with the inoculated medium and poured into sterile Petri dishes. Finally, 5–10 µL of different strains overnight cultures were spotted on the surface of the solidified agar plates (each strain must have the possibility to grow in correspondence with its own spot). The plates were incubated at room temperature until a well-developed lawn of the strain inoculated into grape juice was observed (a week in the case of O. oeni strains). Grape juice was selected as a commercial matrix capable of mimicking the physicochemical conditions of grape must.
As mentioned above, agar diffusion assay has also been performed using wine as substrate, added with 1% yeast extract for all the interactions to test. In this case, the different bacterial strains were pre-stressed in wine and incubated at 30 °C for a week in order to adapt them to the medium promoting their growth: 8 mL of wine (without the addition of yeast extract and pH change) were added to 4 mL of the overnight culture. Furthermore, interactions between all microbial couples were assessed in the red wine while those detected with the first and this method (i.e., in red wine) have also been carried out in white wine in order to evaluate the maintenance of the phenotype as the oenological context varies.

2.5. Interaction Plate Screening: Results Interpretation

It is important to point out that, for both the methodological approaches used in this work, strains seeded through the spots are the ones that eventually interact with the inoculated strain. The presence of interaction has been verified by observing the growth around the spots, which could determine two situations. The lack of growth was displayed by a clear area surrounding the spot, the so-called halo of inhibition, with a diameter proportional to the extent of inhibition itself. On the contrary, a major growth around the spot identifies a positive interaction between the two strains under examination, indicating that the development of the spotted one stimulates the development of the inoculated strain. Otherwise, none of the previous situations occurred if the microbial couple tested does not interact.

3. Results and Discussion

Four categories of microbial interactions, functional to the discussion, can be identified among those tested in this work: yeast-yeast, yeast-bacteria, bacteria-yeast, and bacteria-bacteria. As a whole, negative and neutral interactions have been detected, while no examples of positive interactions have been reported. This is in contrast to the literature in the field, which identifies different behaviors attributable to mutualism/synergism and commensalism reported in matrices of oenological interest [1,54] (e.g., between S. cerevisiae and L. plantarum in grape juices [55], Kloeckera apiculata/S. cerevisiae in grape juice integrated with yeast extract [56]). The findings highlight that plate screening did not seem adequate to detect positive interactions between microorganisms in the wine sector.
Inhibitions representative of all the possible typologies of antagonisms have been observed, including all tested microbial categories (i.e., Saccharomyces/non-Saccharomyces yeasts and lactic acid bacteria). According to the extent of their antagonistic behaviors, the different microorganisms used in this study have been classified as strains of mild (±), middle (+), or strong (++) inhibitory activity showing halos of inhibition, surrounding the respective spots, with a diameter lower than 3 mm, ranging from 3–6 mm or more than 6 mm, respectively. Evidence has been detected in all three media agar used as substrates, resulting in a more frequent on culture medium, followed by grape juice and, finally, wine. In particular, referring to the exerted (Figure 1a) and suffered (Figure 1b) inhibitions, non-Saccharomyces yeasts and LAB showed activity on culture medium and grape juice while S. cerevisiae strains on culture medium and—in only a few cases—wine. These results confirmed, in the oenological field, that in vitro antagonisms do not necessarily correlate with the same behavior in in situ studies [57]. Highlighted trends indicate a selective maintenance of the antagonistic character shifting from tests on a culture medium to evaluation on the edible matrix. Intriguingly, in the case of the yeasts, this selectivity seemed to correspond to the phase of dominance during winemaking: grape juice for non-Saccharomyces and wine for S. cerevisiae [58,59].
Therefore, selected strains belonging to all the microbial categories tested in this plate screening [non-Saccharomyces, S. cerevisiae, and Lactic Acid Bacteria (LAB)] have interacted on culture medium agar (examples in Figure S1).
Evidence highlights only a certain connection with the clear succession of microbial dominance (i.e., non-Saccharomyces in grape must and in early Alcoholic fermentation (AF), Saccharomyces in the middle/late AF, LAB during malolactic fermentation) [30], underlining how the dominance phenomenon is only one of the complex WMC interactions.

3.1. Non-Saccharomyces as Inhibiting Species

Delving into the results found for each of the couple of tested microorganisms, Table 2 shows the inhibitory activity of tested non-Saccharomyces strains against all the studied yeast and bacterial strains.
In literature, several studies deepened the antimicrobial potential of M. pulcherrima (e.g., [27,60]). Interestingly, M. pulcherrima 346, an isolate from commercial starter culture [10], inhibited, on culture medium, bacterial strains representative of spontaneous malolactic consortia (L. plantarum, L. brevis, Pedicoccus spp., and O. oeni) and the autochthonous S. cerevisiae strain I6 [42]. This is consistent with what has been found in previous studies that demonstrated the antimicrobial activity of M. pulcherrima strains against S. cerevisiae, O. oeni, and other lactobacilli of wine interest [37,61,62,63]. Furthermore, these findings could contribute to explaining the modulatory effects on the spontaneous malolactic consortium observed when M. pulcherrima-based commercial starter culture was used in winemaking [30]. On the contrary, the other M. pulcherrima strains exert their antagonistic influence only toward P. fermentans M105A30, in agreement with the evidence observed by Oro et al. [27]. Surprisingly, we found no antimicrobial action on spoilage yeasts Brettanomyces/Dekkera [62]. Taken together, these results proved the strain-dependent character of M. pulcherrima antimicrobial activity. This is probably connected to the intraspecific diversity in terms of the molecular basis responsible for the antagonistic phenotype [64]. The inhibitory activity of M. pulcherrima is addressable to the production of low molecular weight and heat-sensitive metabolites, principally pulcherriminic acid [63]. The acid forms an insoluble red pigment pulcherrimin in the presence of iron (III) ions, with subsequent precipitation. This iron sequestration which depletes the medium of iron, making it unavailable to the other microorganisms’ mechanism appeared to be strain-dependent [64]. Additionally, the inhibition of S. cerevisiae by M. pulcherrima could also come from the competition for nutrients: in the sequential inoculation, the consumption of the nutrients by the non-Saccharomyces yeast at the beginning of AF could prevent the following growth of S. cerevisiae [62].
In this study, T. delbrueckii 291, a commercial strain, showed inhibitory activity toward some bacterial strains on culture medium agar. This might contribute to explaining a negative influence found after inoculation of commercial T. delbrueckii on spontaneous malolactic consortium [30] strains, which is perfectly in accordance with the evidence reported by Nardi et al. [65] that successfully tested the combination of T. delbrueckii and O. oeni strains in red Barbera wine. Together with results reported for M. pulcherrima 346, these findings added a piece to the intricate puzzle of the possible interaction among non-Saccharomyces and malolactic bacteria in oenology [13,28,65,66,67,68,69].
Concerning the other non-Saccharomyces yeasts, some inhibitions on culture medium and grape juice testify to the occurrence of other phenomena of interest. In particular, P. fermentans M105A30 was found largely inhibited. P. fermentans B05A29 displayed a certain negative activity against T. delbrueckii and B. bruxellensis (some Pichia strains have been found to produce a killer toxin called zymocins [70,71]). Finally, all the strains of B. bruxellensis tested in this study inhibited Pediococcus spp. and O. oeni 6 on grape juice agar.

3.2. Saccharomyces as Inhibiting Species

Table 3 reported the inhibitory spectrum of tested Saccharomyces strains with respect to all the studied yeast and bacterial strains.
In this study, the inhibitory activity of S. cerevisiae strains was detected on both culture medium and wine agar. With regard to the first substrate, S. cerevisiae superlievito alcoligens inhibited all the bacterial strains, with the exception of O. oeni strains and L. plantarum T1. These findings confirm the potential of selected S. cerevisiae strains against spoilage LAB in wine [72]. In particular, it was proven the existence of a S. cerevisiae peptidic fraction, with a molecular weight lower than 10 kDa, that inhibits the growth of L. hilgardii [63]. This antagonism could find application also in the reduction of biogenic amines produced by specific L. hilgardii strains in wine [72,73,74]. The trends against L. plantarum strains, but not counter to O. oeni strains, could contribute to explaining the impact of inoculation of the S. cerevisiae selected strain on the spontaneous malolactic consortium [30]. This is an aspect of particular interest if we consider the rising attention delved into L. plantarum as a new species of interest in malolactic control [75]. In general, the evidence confirms the continuous interest in the study of yeast-bacteria compatibility in winemaking [28,69,76].
In this study, it has been detected inhibitory activity of S. cerevisiae T2 toward two other strains of S. cerevisiae: superlievito alcoligens (on wine agar) and on the autochthonous strain I6 (on culture medium and wine agar). This second inhibition represents the only case in which the same inhibition occurred on more than one substrate by means of interactions plate assay in the present study. In the last years, intra-specific inhibitions between different strains of S. cerevisiae have been reported, also with contrasting results in terms of prevalence among wild and commercial S. cerevisiae strains [77,78,79].

3.3. LAB as Inhibiting Species

Interestingly, in this study, the LAB inhibitory activity was detected only on culture medium agar (Table 4).
Excluding a few strains, auto-inhibition was observed among different bacterial species/strains, that are probably addressable to nutrient depletion and acidification [80,81,82]. In this study, Pediococcus spp. inhibited O. oeni OT3. Discordant results concern the couple L. hilgardii—O. oeni, since Rodriguez et al. [83] observed that the growth of O. oeni could be inhibited by means of H2O2 produced by L. hilgardii while, according to Aredes Fernandez et al. [84], the inhibition of O. oeni in co-culture with L. hilgardii seems to be due to competition for arginine, a stimulating agent for the growth of O. oeni, and to the consumption of peptides by L. hilgardii.
Interesting results of this study are referred to the different inhibitions between some LAB and non-Saccharomyces yeasts. Specifically, Pediococcus spp., O. oeni OT3, and O. oeni OT4 inhibited some strains of M. pulcherrima, P. fermentans B05A36, P. fermentans M105A30, and T. delbrueckii 291. Furthermore, O. oeni OT4 has shown inhibitory activity also toward four strains of B. bruxellensis. These last inhibitions are attractive due to the possible application in the biocontrol of this bacterium to inhibit one of the main spoilage agents in wine [32,33].

4. Conclusions

An improved understanding of the interactions among must/wine-associated microorganisms could provide a useful tool to avoid fermentations that are stuck or sluggish, optimize wine quality/safety, and minimize the production of those compounds that depreciate wine quality. From this point of view, the study (i) characterized the in vitro potential of microbial resources that might be exploited for biocontrol activities on grape/wine and (ii) provided original information that can contribute to explaining a range of microbial interactions in the oenological trials. However, this reservoir of microbial antagonisms was drastically reduced when tested on the real matrices (must and wine). As said, it was possible to observe a considerable number of inhibitions exerted by non-Saccharomyces strains (on grape juice) and a few inhibitions by S. cerevisiae (on wine). This is consistent with the broader challenge in dealing with the exploitation of microbial controlling traits directly in situ in the food industry [85,86]. It is important to underline that the interactions studied in this paper are related to the growth/no growth of microorganisms, with research activities that are propaedeutic to but not considering the metabolic interaction, which is one of the current trends in wine microbiological studies (see [87,88,89,90]). Highlighted microbial interactions are very important for the sustainable control of spoilage yeasts and the management of alcoholic fermentation, malolactic fermentation, and the development of a distinctive aroma profile [71]. In addition, the plate assay method could be a fast, cheap, and suitable method to exclude negative interactions among Saccharomyces spp., NSY, and malolactic bacteria during trials from regional spontaneous fermentations with the aim to select tailored mixed starter cultures [42,91].

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app122412760/s1, Figure S1: inhibitions tests on agarised grape juice.

Author Contributions

Conceptualisation, M.D.G., P.R., M.F., F.G., G.S. and V.C.; Methodology, M.D.G., P.R., N.D.S., F.G., M.F., G.S. and V.C.; Investigation, M.D.G., P.R., N.D.S. and M.F.; Resources, G.S. and V.C.; Data curation, M.D.G., P.R., M.F. and V.C.; Writing—original draft preparation, M.D.G., M.F., P.R. and V.C.; Writing—review and editing, N.D.S., F.G. and G.S.; Supervision, P.R., M.F., F.G., G.S. and V.C.; Project administration, P.R., F.G., G.S. and V.C.; Funding acquisition, G.S., F.G., and V.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was partially supported by the Apulia Region Projects: “Innovazione nella tradizione: tecnologie innovative per esaltare le qualità dei vini autoctoni spumante della murgia barese—INVISPUBA” and “Spumantizzazione e frizzantatura per il rilancio della vitivinicoltura dell’areale Centro Nord della regione Puglia—SPUMAPULIA” (P.S.R. Puglia 2014/2020-Misura 16.2).

Acknowledgments

The authors acknowledge Massimo Franchi, Domenico Genchi, Pasquale Del Vecchio and Giuseppe Panzarini of the Institute of Sciences of Food Production—CNR for the skilled technical support provided during the realizations of this work.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 12760 g001 550
Figure 1. Frequency of inhibitory activity concerning the inhibiting (a) and inhibited (b) species, according to the different media tested.
Figure 1. Frequency of inhibitory activity concerning the inhibiting (a) and inhibited (b) species, according to the different media tested.
Applsci 12 12760 g001
Table
Table 1. List of microorganisms of enological interest used in this work.
Table 1. List of microorganisms of enological interest used in this work.
SpeciesStrain CodeMatrix/Source
Saccharomyces cerevisiaesuperlievito alcoligensCSC
S. cerevisiaeeleganceCSC
S. cerevisiae ex bayanusEC1118CSC
S. cerevisiaeE4OSF
S. cerevisiaeI6OSF
S. cerevisiaeSUPRARED HGCSC
S. cerevisiaeT2CSC
Hanseniaspora uvarum1444CECT
H. uvarumB05B29OSF
Hanseniaspora guilliermondiiM105A31OSF
Torulaspora delbrueckii11199CECT
T. delbrueckiiB05B12OSF
T. delbrueckii291CSC
Pichia fermentansM105A3OSF
P. fermentansB05A36OSF
P. fermentansB05A29OSF
Issatchenkia terricolaB05B8OSF
Starmerella bacillarisB05B6OSF
Metschnikowia pulcherrimaB0512B3OSF
M. pulcherrimaB0512B24OSF
M. pulcherrimaB0512B25OSF
M. pulcherrimaB0512B26OSF
M. pulcherrimaB0512B15OSF
M. pulcherrimaB05B2POSF
M. pulcherrimaB05A36OSF
M. pulcherrimaM105A51OSF
M. pulcherrimaB0522OSF
M. pulcherrima346CSC
Brettanomyces bruxellensis2OSF
B. bruxellensis4OSF
B. bruxellensis5OSF
B. bruxellensis6OSF
B. bruxellensis7OSF
Lactiplantibacillus plantarumLp90OSF
L. plantarum44OSF
L. plantarumV22CSC
L. plantarum38 CDSOSF
L. plantarumT1OSF
Levilactobacillus brevis9809IOEB
Lentilactobacillus hilgardii4786CECT
Pediococcus parvulus126OSF
Pediococcus spp.32OSF
Oenococcus oeniOT3OSF
O. oeni6OSF
O. oeniOT4OSF
OSF, oenological spontaneous fermentation, UNIFG collection; CSC, commercial starter culture; CECT, Colección Española de Cultivos Tipo; IOEB, Bacteria collection of the “Faculté d’Oenologie de Bordeaux”.
Table
Table 2. Inhibitory activity of non-Saccharomyces yeasts according to the diameter of halo of inhibition: “±” = lower than 3 mm, “+” = ranging from 3–6 mm and “++” = more than 6 mm.
Table 2. Inhibitory activity of non-Saccharomyces yeasts according to the diameter of halo of inhibition: “±” = lower than 3 mm, “+” = ranging from 3–6 mm and “++” = more than 6 mm.
Inhibiting SpeciesInhibited SpeciesInhibitory Activity
M. pulcherrima 346S. cerevisiae I6± C
L. plantarum V22± C
L. brevis IOEB± C
L. plantarum 38 CDS± C
Pediococcus spp.± C
O. oeni OT3± C
T. delbrueckii 291L. plantarum Lp90++ C
L. plantarum 44++ C
L. brevis IOEB++ C
P. parvulus 126++ C
L. hilgardii CECT 4786++ C
L. plantarum 38 CDS++ C
Pediococcus spp.± C
P. fermentans M105A30Pediococcus spp.± C
P. fermentans B05A36Pediococcus spp.± C
H. guilliermondii M105A31P. fermentans M105A30± J
H. uvarum B05B29P. fermentans M105A30± J
P. fermentans B05A29T. delbrueckii 291± J
T. delbrueckii CECT 11199± J
B. bruxellensis 2± J
B. bruxellensis 6± J
M. pulcherrima B0512B3P. fermentans M105A30± J
M. pulcherrima B0512B24P. fermentans M105A30± J
M. pulcherrima B0512B25P. fermentans M105A30± J
M. pulcherrima B0512B26P. fermentans M105A30± J
M. pulcherrima B0512B15P. fermentans M105A30± J
M. pulcherrima B05B2PP. fermentans M105A30± J
M. pulcherrima B05A36P. fermentans M105A30± J
M. pulcherrima B0522P. fermentans M105A30± J
B. bruxellensis 2Pediococcus spp.++ J
O. oeni 6++ J
B. bruxellensis 4Pediococcus spp.± J
O. oeni 6+ J
B. bruxellensis 5Pediococcus spp.± J
O. oeni 6+ J
B. bruxellensis 6Pediococcus spp.± J
O. oeni 6+ J
B. bruxellensis 7Pediococcus spp.± J
O. oeni 6+ J
The superscripts indicate the medium onto which the results have been observed: “C” = culture medium and “J” = grape juice.
Table
Table 3. Inhibitory activity of S. cerevisiae strains according to the diameter of halo of inhibition: “±” = lower than 3 mm, “+” = ranging from 3–6 mm and “++” = more than 6 mm.
Table 3. Inhibitory activity of S. cerevisiae strains according to the diameter of halo of inhibition: “±” = lower than 3 mm, “+” = ranging from 3–6 mm and “++” = more than 6 mm.
Inhibiting SpeciesInhibited SpeciesInhibitory Activity
S. cerevisiae T2S. cerevisiae superlievito alcoligens± W
S. cerevisiae I6± C,W
S. cerevisiae superlievito alcoligensL. plantarum Lp90++ C
L. plantarum 44++ C
L. plantarum V22++ C
L. brevis IOEB++ C
P. parvulus 126++ C
L. hilgardii CECT 4786++ C
L. plantarum 38 CDS++ C
The superscripts indicate the medium onto which the results have been observed: “C” = culture medium and “W” = wine.
Table
Table 4. Inhibitory activity of lactic bacteria species according to the diameter of halo of inhibition: “±” = lower than 3 mm, “+” = ranging from 3–6 mm and “++” = more than 6 mm.
Table 4. Inhibitory activity of lactic bacteria species according to the diameter of halo of inhibition: “±” = lower than 3 mm, “+” = ranging from 3–6 mm and “++” = more than 6 mm.
Inhibiting SpeciesInhibited SpeciesInhibitory Activity
L. plantarum Lp90L. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
L. plantarum 44L. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
L. plantarum V22L. plantarum Lp90+ C
L. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
L. brevis IOEBL. plantarum Lp90+ C
L. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
P. parvulus 126L. plantarum Lp90+ C
L. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
L. hilgardii CECT 4786L. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
L. plantarum 38 CDSL. plantarum 44± C
L. plantarum V22± C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS+ C
Pediococcus spp.± C
L. plantarum T1L. plantarum Lp90++ C
L. plantarum 44++ C
L. brevis IOEB++ C
P. parvulus 126++ C
L. plantarum 38 CDS++ C
Pediococcus spp.+ C
Pediococcus spp.O. oeni OT3+ C
L. plantarum Lp90++ C
L. plantarum 44+ C
L. plantarum V22++ C
L. brevis IOEB± C
P. parvulus 126+ C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS++ C
M. pulcherrima B0512B3± C
M. pulcherrima B0512B25± C
P. fermentans M105A30++ C
P. fermentans B05A36++ C
T. delbrueckii 291++ C
O. oeni OT3O. oeni OT3+ C
L. plantarum Lp90++ C
L. plantarum 44+ C
L. plantarum V22++ C
L. brevis IOEB± C
P. parvulus 126± C
L. hilgardii CECT 4786± C
L. plantarum 38 CDS++ C
M. pulcherrima B0512B3± C
M. pulcherrima B0512B25± C
M. pulcherrima B0512B26± C
M. pulcherrima B0522± C
P. fermentans M105A30+ C
P. fermentans B05A36++ C
T. delbrueckii 291+ C
O. oeni 6O. oeni OT3± C
O. oeni OT4O. oeni OT3± C
M. pulcherrima B0512B3± C
P. fermentans M105A30++ C
P. fermentans B05A36± C
T. delbrueckii 291++ C
B. bruxellensis 2+ C
B. bruxellensis 4± C
B. bruxellensis 6± C
B. bruxellensis 7± C
The superscript indicates the medium onto which the results have been observed: “C” = culture medium.
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De Gioia, M.; Russo, P.; De Simone, N.; Grieco, F.; Spano, G.; Capozzi, V.; Fragasso, M. Interactions among Relevant Non-Saccharomyces, Saccharomyces, and Lactic Acid Bacteria Species of the Wine Microbial Consortium: Towards Advances in Antagonistic Phenomena and Biocontrol Potential. Appl. Sci. 2022, 12, 12760. https://doi.org/10.3390/app122412760

AMA Style

De Gioia M, Russo P, De Simone N, Grieco F, Spano G, Capozzi V, Fragasso M. Interactions among Relevant Non-Saccharomyces, Saccharomyces, and Lactic Acid Bacteria Species of the Wine Microbial Consortium: Towards Advances in Antagonistic Phenomena and Biocontrol Potential. Applied Sciences. 2022; 12(24):12760. https://doi.org/10.3390/app122412760

Chicago/Turabian Style

De Gioia, Marianna, Pasquale Russo, Nicola De Simone, Francesco Grieco, Giuseppe Spano, Vittorio Capozzi, and Mariagiovanna Fragasso. 2022. "Interactions among Relevant Non-Saccharomyces, Saccharomyces, and Lactic Acid Bacteria Species of the Wine Microbial Consortium: Towards Advances in Antagonistic Phenomena and Biocontrol Potential" Applied Sciences 12, no. 24: 12760. https://doi.org/10.3390/app122412760

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