Colonization of the human gut by bovine bacteria present in Parmesan cheese.

Discipline: microbiology; Key words: Parmesan cheese, organoleptic features, microbiota, gut colonization.

Bacteria are ubiquitous microorganisms present in all known environments, including various areas of the animal body as well as in fermented dairy foods, where they are organized in complex consortia. The microbial ecology of fresh cheese has been extensively investigated, and has lead to the generally accepted understanding that bacteria residing in milk may contribute beneficially to the aroma of fermented dairy products. Here, lactic acid bacteria are particularly important due to their positive or negative impacts on fresh and ripened cheese. Milk, on the other hand, is an important vector for transmission of bacteria from mother to newborn, thereby promoting establishment of the early microbiota in the essentially sterile gut of newborn mammals. From milk to cheese, however, little is known about the transfer of cow-derived microbiota transmission of a consortium of bacteria along the food chain, and as a result, to the consumer. Therefore, in a study by Dr C. Milani and co-workers, a microbial ecology-based approach was applied to elucidate the bacterial transmission down to strain level along the production chain of Parmesan cheese, including consumers of the latter product. They published their results open ended in NATURE COMMUNICATIONS | (2019) 10:1286 | https://doi.org/10.1038/s41467-019-09303-w | www.nature.com/naturecommunications, the title being: Colonization of the human gut by bovine bacteria present in Parmesan cheese. 

To investigate the taxonomic composition of the bacterial populations associated with the production chain of Parmesan cheese, the researchers collected a set of samples from five cheese making sites which are located in distinct geographical areas in the provinces of Parma and Reggio Emilia in Italy. Each sample set consisted of ten dairy cattle faecal samples, ten cattle litter samples and three samples of Parmesan Cheese at one day of ripening for a total of 165 samples corresponding to 33 samples per cheese making site. Each collected sample was subjected to 16S rRNA gene-based microbial profiling through Illumina sequencing, resulting in a total of 11,622,668 sequenced reads. The evaluation of the bacterial biodiversity for each sample was performed by alpha diversity analysis based on the construction of rarefaction curves using 10 data sub-sampling points, as well as on assessment of the Chao1 and Shannon indexes. To evaluate if bacteria transmitted across the Parmesan cheese production chain can colonize and persist in the human gut, an in vivo pilot study involving a total of 20 healthy individuals was performed. The enrolled subjects were requested to eat the recommended daily dose of fresh Parmesan cheese, i.e., 45 g per day, for seven days. Each enrolled individual was provided with seven 45 g portions obtained from the same cheese produced in one plant. The presence of the chosen indicator strain B. mongoliense BMONG18 in the portioned fresh Parmesan cheese was verified using a strain-specific primer pair. These primers were also used to evaluate the presence and absolute abundance of B. mongoliense BMONG18, by means of qPCR, in the stool samples of the 20 enrolled individuals during Parmesan cheese consumption and for seven subsequent days.  

The data represent the first strain-level validation of transmission of bacteria across the Parmesan cheese production chain and reveals that (fresh) cheese may act as a transmission vehicle of such bacteria to humans. This probably will have a major impact on the genomic diversity in the developing microbiota during early life. Moreover, the presence of dairy cattle’s gut and milk bacteria in cheese, along with some environmental bacteria, may be pivotal to understand the peculiar organoleptic features that distinguish the cheese made by different producers, since such bacteria may be expected to play a role in cheese ripening and maturation. Altogether, the results suggest a genetic adaptation of B. mongoliense BMONG18 to bovine milk and that this nutritious fluid activates gut colonization of and host communication by this species.  

Implications of the study: Bacteria harboured by the bovine gut microbiota or by the housing environment, modulate the microbiota of milk and, consequently, the corresponding cheese. Moreover, bacteria harboured by Parmesan cheese may colonize and persist in the gut of those individuals who consume this cheese on a daily basis. The study furthermore implicated that daily consumption of milk may support the engraftment of bacteria transmitted across the Parmesan cheese production chain to the human gut and suggests the existence of co-operative behaviour between certain food-vectored bacteria. Altogether, these results highlight that a thorough understanding of the mechanisms responsible for the origin of the cheese microbiota will be pivotal to appreciate its impact on the complex ecological relations between bacterial populations harboured by the gut of cheese consumers, with possible positive implications to human health.