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. 2020 Jun 17;9(6):797.
doi: 10.3390/foods9060797.

Effect of Biofilm Formation by Lactobacillus plantarum on the Malolactic Fermentation in Model Wine

Gianfranco Pannella  1 , Silvia Jane Lombardi  1 , Francesca Coppola  2 , Franca Vergalito  1 , Massimo Iorizzo  1 , Mariantonietta Succi  1 , Patrizio Tremonte  1 , Caterina Iannini  1 , Elena Sorrentino  1 , Raffaele Coppola  1
Affiliations

Effect of Biofilm Formation by Lactobacillus plantarum on the Malolactic Fermentation in Model Wine

Gianfranco Pannella et al. Foods. .

Abstract

Biofilm life-style of Lactobacillus plantarum (L. plantarum) strains was evaluated in vitro as a new and suitable biotechnological strategy to assure L-malic acid conversion in wine stress conditions. Sixty-eight L. plantarum strains isolated from diverse sources were assessed for their ability to form biofilm in acid (pH 3.5 or 3.2) or in ethanol (12% or 14%) stress conditions. The effect of incubation times (24 and 72 h) on the biofilm formation was evaluated. The study highlighted that, regardless of isolation source and stress conditions, the ability to form biofilm was strain-dependent. Specifically, two clusters, formed by high and low biofilm producer strains, were identified. Among high producer strains, L. plantarum Lpls22 was chosen as the highest producer strain and cultivated in planktonic form or in biofilm using oak supports. Model wines at 12% of ethanol and pH 3.5 or 3.2 were used to assess planktonic and biofilm cells survival and to evaluate the effect of biofilm on L-malic acid conversion. For cells in planktonic form, a strong survival decay was detected. In contrast, cells in biofilm life-style showed high resistance, assuring a prompt and complete L-malic acid conversion.

Keywords: acid stress; biological decarboxylation; ethanol stress; wood attached cells.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Heat-map related to the production of biofilm (expression) determined on 68 L. plantarum strains from different matrices (origin). The strains were grown for 24 h at 28 °C under different stress conditions (type): in Man Rogosa Sharpe (MRS) broth (control), in MRS broth at pH 3.5 (pH 3.5), in MRS broth at pH 3.2 (pH 3.2), and in MRS broth containing ethanol at 12% (Et12) or ethanol at 14% (Et14).
Figure 2
Figure 2
Principal component analysis (PCA) biplot of the first two principal components grouped (groups) by matrix of isolation.
Figure 3
Figure 3
Effect of incubation time (24 h vs. 72 h) on L. plantarum biofilm formation. Strains are grouped in high (H) and low (L) biofilm producers. * indicates significant differences (p < 0.05). OD, optical density.
Figure 4
Figure 4
Biofilms produced (biofilm_score) by high producer strains of L. plantarum after 24 h and 72 h of incubation in MRS broth in presence of acid stress (pH 3.5 pH 3.2), ethanol stress (Et12, Et14) or without stress (control). The biofilm_score value is the ratio between the median values of crystal violet (CV) OD620 (median values of OD620 calculated on cells in biofilm form) and OD620 (median values of OD620 calculated on cells in planktonic form).
Figure 5
Figure 5
Mean values with standard deviation of L. plantarum strains belonging to high biofilm producer group. Cells were enumerated in the biofilms of 24 and 72 h, formed in MRS broth in presence of acid stress (pH 3.5, pH 3.2), ethanol stress (Et12, Et14), or without stress (control). Different letters indicate significant differences (p < 0.05).
Figure 6
Figure 6
Density plot of biofilm_expression and biofilm_score indices of high biofilm L. plantarum producer strains.
Figure 7
Figure 7
Survival of planktonic cells, biofilm cells, detached cells from biofilm, and pre-adapted cells of L. plantarum Lpls22 inoculated at high concentration in MW at (A) pH 3.5 and (B) pH 3.2. Trend of L-malic and L-lactic acid in MW at (C) pH 3.5 and (D) pH 3.2 inoculated with biofilm cells, planktonic cells, or pre-adapted cells of L. plantarum Lpls22. Data are reported as mean values with standard deviation of three biological replicates. * indicates significant (p < 0.05) differences compared with 0 h. # indicates significant (p < 0.05) differences compared with pre-adapted cells at the same time.
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