An integrated multi-omics framework reveals ecological and metabolic drivers of biogenic amine accumulation in cheese

In this study, a multi-omics approach was applied to integrate microbial community profiling, volatile metabolite analysis and multivariate statistics, with the aim of exploring the factors associated with biogenic amines accumulation in cheeses. Thirty-three cheeses produced in Italy and France were classified according to milk origin and cheesemaking technology into four categories, i.e. i) bovine Hard Cheeses, ii) bovine Soft Cheeses, iii) bovine Pasta Filata cheeses, and iv) Non-Bovine cheeses. Biogenic amine concentrations varied markedly among cheese types. Non-bovine cheeses, showed overall the highest BA levels, mainly driven by tyramine, cadaverine and putrescine. In contrast, Pasta Filata cheeses generally displayed the lowest biogenic amine concentrations, whereas Hard Cheeses showed a wide variability, not strictly associated with ripening time. The 16rRNA sequencing showed how the microbial community was largely sample-dependent, although Enterococcus, Carnobacterium and several Enterobacteriaceae, were associated with cheeses richer in biogenic amines. Volatile organic compounds profiling further highlighted metabolic differences among cheese categories, with specific carboxylic acids, esters and ketones contributing to sample discrimination. Multivariate integration of microbial, metabolite and amines data suggested that biogenic amines accumulation is mainly linked to the metabolic and ecological configurations of cheese microbiota rather than to the presence of single aminogenic species. Overall, the results indicate that BA formation in cheese reflects complex interactions between microbial communities, technological practices and ripening conditions, highlighting the importance of an ecosystem-level perspective in understanding BA variability in traditional cheeses.