Microbial community dynamics in a traditional Swiss mountain cheese over 142 years of cheesemaking

Abstract

The history of cheesemaking is deeply intertwined with the evolution of microbial communities, from spontaneous fermentation to modern, standardized practices. Despite centuries of refinement, the most profound shifts in cheese production occurred in the last century, driven by advances in microbiology and production technologies. These changes have shaped the bacterial and viral communities within cheese, yet the specific impacts remain underexplored. Using shotgun metagenomics and 16S rRNA gene amplicon sequencing approaches, we examined microbial community changes in Raclette du Valais, a traditional Swiss cheese, using preserved cheese wheels from 1875 to 2017 from the same alpine dairy in Switzerland. Our results reveal that significant shifts in microbial community composition coincide with changes in production practices. Notably, the oldest cheese harbored a distinct bacterial community, dominated by Lactiplantibacillus paraplantarum, Streptococcus thermophilus, Pseudolactococcus laudensis, and taxa commonly associated with the gut environment, indicative of spontaneous fermentation and the use of calf stomach for milk coagulation. Functionally, we can also track the rise and fall of antibiotic resistance genes mirroring their use. Furthermore, we found that domestication of lactic acid bacteria predates the studied period, and that bacteriophage genera detected in 1875 are representatives of those commonly found in modern cheesemaking. These findings highlight how microbial communities have adapted to changing production methods and how human intervention, through practices like antibiotic use in animal husbandry, has influenced these ecosystems in remote alpine cheesemaking. Significance StatementCheesemaking relies on complex microbial ecosystems shaped by long-standing human practices, yet how these communities responded to the modernization of food production has remained largely unknown. By analyzing DNA preserved in historical cheese wheels from a single alpine dairy, we examine microbial community changes across a key technological transition. We show that modernization impacted bacterial composition and functional potential, that cheese microbiomes record the rise of agricultural antibiotic use, and that major cheese-associated phages and domesticated starter bacteria were already established over a century ago. These findings demonstrate that historical cheeses preserve long-term microbial records and offer a glimpse how changes in food production practices shape fermented-food microbiomes.