Metagenomic profiling reveals how ecological and processing drivers shape the beef microbiome from farm to fork

Meat processing environments harbor complex microbial ecosystems that may be transferred to the final product, thus influencing product quality and safety. Several factors may affect microbiome composition, such as seasonality and sanitation procedures. In this study, we carried out a metagenomic analysis over two seasons across four beef processing facilities, following beef carcasses from farm-to-fork. The pre-maturation environment was dominated by Corynebacterium xerosis and Acinetobacter johnsonii in summer, and by Bifidobacterium pseudolongum and Cutibacterium acnes in winter, whereas meat maturation environments were colonized by a specialized lactic acid bacterial community. The long-term maturation stage was led by Carnobacterium divergens and Carnobacterium maltaromaticum, whereas Pseudolactococcus carnosus and Pseudolactococcus paracarnosus prevailed during the retail stage. The environmental microbiome exhibited broad metabolic potential, in contrast to the specialized, low-diversity profiles of mature meat. Routine sanitation practices did not fully remove detectable microbial DNA signatures from environmental surfaces and were associated with shifts in taxonomic and functional profiles, including a greater representation of biofilm-associated genes. We also identified a diverse phage community, and statistical modeling revealed strong negative predictive associations with Listeria monocytogenes, Salmonella enterica, and Staphylococcus aureus. Collectively, our findings demonstrate that the beef processing microbiome is shaped by the interaction of multiple ecological forces. Understanding these interactions provides a comprehensive framework for ecology-based strategies to improve meat quality, safety, and shelf-life.