Environmental sources along natural cave ripening shape the microbiome and metabolome of artisanal blue-veined cheeses

Abstract Microorganisms colonising processing environments can significantly impact food quality and safety.Here we describe a detailed longitudinal study assessing the impact of cave ripening on the microbial succession and cheese metabolome across different producers of Cabrales blue-veined cheese. Both the producer and cave in which cheeses were ripened significantly influenced the cheese microbiome and metabolome. Lactococcus and the fomer Lactobacillus genus, among other taxa, showed high abundance in cheeses at initial stages of ripening, either coming from the raw material, starter culture used and/or the environment of processing plants. Along cheese ripening in caves, these taxa were displaced by other bacteria, such as Tetragenococcus, Corynebacterium, Brevibacterium, Yaniella and Staphylococcus, predominantly originating from cave environments (mainly food contact surfaces), as demonstrated by source tracking analyses, strain analysis at read level and the characterization of 613 metagenome assembled genomes. Tetragenococcus koreensis and T. halophilus were detected at high abundance in cheese and Tetragenococcus showed a high level of horizontal gene transfer with other members of the cheese microbiome, mainly with Lactococcus and Staphylococcus, involving genes related to carbohydrate metabolism functions, indicating that these transfer events may have mediated the adaptation of Tetragenococcus to the dairy environments. Overall, we demonstrated that processing environments can be a source of non-starter microorganisms of relevance to ripening of artisan fermented foods, we identified novel taxa not previously regarded as being dominant components of the cheese microbiome (Tetragenococcus spp.), providing very valuable information to the authentication of this Protected Designation of Origin artisanal cheese in the future.