Phages Shape Microbial Dynamics and Metabolism of a Model Community Mimicking Cider, a Fermented Beverage

Model microbial communities are often studied to better understand interactions and fluxes during fermentation processes. However, models that take into account the potential impact of bacteriophages (phages), which are recognized as drivers of microbial communities, are scarce, especially in fermented foods. This study aimed at investigating the behavior of a cider model microbial community, which was subjected to disturbance in the presence or absence of phages and at two different temperatures (25 °C and 15 °C). The model microbial community was composed of three lactic acid bacteria (LAB) strains belonging to the species Liquorilactobacillus mali, Leuconostoc mesenteroides and Oenococcus oeni, and of a Saccharomyces uvarum yeast strain. Two phages were selected, targeting L. mali and Ln. mesenteroides strains. In order to follow the behavior of the microbial community model, the phages and microbial strains were enumerated at several time points, and the metabolic signatures (sugar consumption, production of organic acids and volatile organic compounds) of the model microbial community were monitored. At 25 °C, the community with phages (P) was significantly closer to the control condition (C) than to the condition without phages (D). Microbial levels were similar between conditions C and P, which were characterized by high concentrations of compounds such as 2-phenylethanol, ethyl octanoate and isoamyl alcohol, and more globally by a more complex metabolic signature than that of condition D. In condition D, L. mali and Ln. mesenteroides were dominant while S. uvarum and O. oeni were less present, and this condition was characterized by a high concentration of ethyl lactate. At 15 °C, condition P differed from conditions C and D, as Ln. mesenteroides was not detected while the other strains all reached approximately the same levels. The metabolic range of condition P was less important than for conditions C and D. The current study showed that the influence of phages on the model microbial community dynamics and metabolisms after a disturbance phenomenon was temperature-dependent.