Microbe-Microbe Interaction Between Staphylococcus aureus and Lactic Acid Bacteria Resulting in a Reshuffle of the Microbial Metabolisms and Prevention of Staphylococcal Enterotoxin Production

In complex microbial ecosystems, microorganisms interact and communicate resulting in a series of phenomena, which may lead to dominance, coexistence, and limitation of one species with respect to others. In food microbiology, this aspect assumes specific interest (e.g., when a pathogenic microorganism represents one member of the consortium), as its pathogenic potential may be impaired by the interaction with the food microbiota. In this study, we investigated the interaction between Staphylococcus aureus and Enterococcus faecalis in milk using phenotypical and molecular approaches. Staphylococcus aureus ATCC 29213 was grown in pure culture or in the presence of a cheese-isolated E. faecalis in skimmed milk. Enterotoxin was not produced in co-culture and S. aureus population decrease one-log in comparison to single culture. RNA-Seq analysis highlighted deep alterations in the S. aureus transcriptome during exponential and stationary growth in co-culture with E. faecalis. Several genes were fully repressed in co-culture, including the agr, sar-family and mgrA global regulators; and, as a consequence, several agr-regulated exoproteins. In contrast, expression of genes coding for surface proteins (spa, clfB, sdrD, sdrE, sasF, sasG, sasH) was increased in co-culture, probably due to the loss of agr influence. Interestingly, we observed significant modifications in the transcription of several metabolite-responsive elements, such as ccpA, ccpE and codY, and genes involved in glycolysis and pyruvate metabolism. The present study demonstrates that S. aureus virulence and metabolism are profoundly impacted by the presence of E. faecalis in a simulated food ecosystem and it provides relevant evidence to better understand the pathogen-lactic acid bacteria interactions in foods.