Linking the genome of lactic acid bacteria to the metabolic response of humans having ingested fermented dairy products

Guy Vergères, Agroscope, Institute for Food Sciences, Berne, Switzerland

Fermentation is a major transformation process in the food and beverage industry and up to one third of products consumed worldwide are fermented. Humans have been fermenting foods and beverages since at least seven millennia, first to protect them from microbial spoilage, later to provide them with attractive sensory properties. This dietary behavior is likely to have impacted on physiological functions other than olfactory processes. Only recently in human history, in particular with the pioneering work of Metchnikoff at the beginning of the 20th century, has food fermentation been considered from the point of view of health benefits. This initial research has later evolved into the field of probiotics. Probiotic research is, however, still struggling on how to translate scientifically sound data into clinically relevant information. In this context, the recently gained knowledge on the key role of the gut microbiome on human health is triggering a scientific renewal, shifting research questions from the search for specific properties of individual bacterial strains to the importance of gut microbial diversity. Taken together, the current knowledge suggests that diets rich in fermented foods may support health by delivering a diverse pool of bioactive compounds (bacteria, bacterial metabolites, products of fermentation) to the gastrointestinal tract and, eventually, to the organism. Milk is a strategic vector to deliver bacteria and bacterial products to the human organism, in particular because of the acceptance of fermented dairy products by consumers but also, from a technological point of view, because of the sustainability of the fermentation process. We have therefore conducted a series of four acute and short-term intervention studies investigating the response of healthy human subjects to a range of dairy products, including milk, yoghurt, cheese, and butter. The analytical strategy taken to investigate these interactions included a high-density data characterization of the ingested food products (foodomics) as well as of the human samples collected during the intervention (nutrigenomics). Dairy products were characterized both microbiologically, by sequencing the genomic content of the fermenting strains of lactic acid bacteria (LAB), and chemically by measuring their metabolomes. On the other hand, the response of the subjects to the ingestion of the dairy products was investigated by measuring the serum and urine metabolomes, the blood cell transcriptome, and the fecal microbiome. These datasets were complemented with validated metabolic and inflammatory blood parameters. Analyses of the metabolomes of both the dairy matrices and human samples allowed the identification of metabolites whose appearance in humans could directly be attributed to the fermentation of milk to dairy products. The microbial composition of the fecal microbiome was also modified when the ingested dairy matrix was technologically modified, indicating an impact on the composition of the gastrointestinal microbial community. Also, the postprandial blood cell transcriptome of the subjects responded differentially to the ingestion of the processed foods.

Finally, sequencing the genome of a range of LABs suggested that genetic information can be linked to the metabolome of the corresponding fermented milk products, thus opening the door to screening strategies for LABs aimed at increasing metabolic diversity in fermented dairy products.

Using this panel of analyses, we were able to provide a proof of concept for an analytical strategy that links the genomic content of LABs to the metabolic response of subjects having ingested the corresponding fermented dairy products. This link remains, however, thin. A holistic understanding of these interactions will not only require an in depth analysis of the biological information contained in the living organisms used in our studies (LAB and humans) but should also be complemented by additional research initiatives.

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