Dynamics of the viral community on the cheese surface during maturation and persistence across production years

Abstract

ABSTRACTThe surface of smear-ripened cheeses constitutes a dynamic microbial ecosystem resulting from the successive development of different microbial groups. Recent studies indicate that a viral community, mainly composed of bacteriophages, coexists with cellular microorganisms in this ecosystem, but its ecological significance remains to be elucidated. In this work, we studied a French smear-ripened cheese by both viral metagenomics and 16S metabarcoding approaches to assess both the dynamics of phages and bacterial communities on the cheese surface during the ripening period, and their persistence in ready-to-eat cheeses over the years of production. We observed a clear transition of the phage community structure during ripening with a decreased relative abundance of viral species (vOTUs) associated withLactococcusphages, which were replaced by vOTUs associated with phages infecting ripening bacteria such asBrevibacterium, Glutamicibacter, PseudoalteromonasandVibrio. The dynamics of the phage community was strongly associated with bacterial successions observed on the cheese surface. Finally, a core of abundant vOTUs were systematically detected in ready-to-eat cheeses produced at different dates spanning more than 4 years of production, indicating long-term persistence of the main phages in the cheese production environment. Together, these findings offer novel perspectives on the ecology of bacteriophages in smear-ripened cheese and emphasize the significance of incorporating bacteriophages in the microbial ecology studies of fermented foods.IMPORTANCESmear-ripened cheeses are microbial ecosystems made up of various microorganisms including bacteria, yeasts and also viruses such as bacteriophages, which infect and regulate bacterial populations. In this work, a French smear-ripened cheese was used to study how these viruses and bacteria interact over time and during cheese production. It revealed that the composition of the bacteriophage community shifts during the ripening process, aligning with the bacterial successions observed on the cheese surface between lactic acid bacteria and ripening bacteria. Additionally, the vast majority of these bacteriophages were found consistently in cheese products made over a 4-years period, showing that they represent a persistent component of the cheese-making environment. This research highlights the importance of considering these bacteriophages when studying the microbial life of fermented foods like cheese.