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Review 1: "Dynamics of the Viral Community on the Cheese Surface during Maturation and Persistence across Production Years"

The reviewer highlighted the study's potential impact on the dairy sector, starter culture industry, and food policy makers, particularly in demonstrating the importance of bacteriophages in fermented food microbiology beyond lactic acid bacteria.

Published onJul 01, 2024
Review 1: "Dynamics of the Viral Community on the Cheese Surface during Maturation and Persistence across Production Years"
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Dynamics of the viral community on the surface of a French smear-ripened cheese during maturation and persistence across production years
Dynamics of the viral community on the surface of a French smear-ripened cheese during maturation and persistence across production years
Description

ABSTRACT The surface of smear-ripened cheeses constitutes a dynamic microbial ecosystem resulting from the successive development of different microbial groups such as lactic acid bacteria, fungi and ripening bacteria. Recent studies indicate that a viral community, mainly composed of bacteriophages, also represents a common and substantial part of the cheese microbiome. However, the composition of this community, its temporal variations and associations between bacteriophages and their hosts remain poorly characterized. Here, we studied a French smear-ripened cheese by both viral metagenomics and 16S metabarcoding approaches to assess both the succession of phages and bacterial communities on the cheese surface during cheese ripening, and their temporal variations 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 with Lactococcus phages, which were replaced by vOTUs associated with phages infecting ripening bacteria such as Brevibacterium, Glutamicibacter, Pseudoalteromonas and Vibrio. The dynamics of the phage community was strongly associated with bacterial successions observed on the cheese surface. Finally, while some variations in the distribution of phages were observed in ready-to-eat cheeses produced at different dates spanning more than 4 years of production, the most abundant phages were detected throughout. This result revealed the long-term persistence of the dominant 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.IMPORTANCE The succession of diverse microbial populations is critical for ensuring the production of high-quality cheese. We observed a temporal succession of phages on the surface of a smear-ripened cheese, with new phage communities showing up at the time when ripening bacteria start covering this surface. Interestingly, the final phage community of this cheese is also consistent over large periods of time, as the same bacteriophages were found in cheese products from the same manufacturer made over 4-years. This research highlights the importance of considering these bacteriophages when studying the microbial life of fermented foods like cheese.

RR:C19 Evidence Scale rating by reviewer:

  • Strong. The main study claims are very well-justified by the data and analytic methods used. There is little room for doubt that the study produced has very similar results and conclusions as compared with the hypothetical ideal study. The study’s main claims should be considered conclusive and actionable without reservation.

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Review: The authors studied French smear-ripened cheeses by both viral metagenomics and 16S metabarcoding approaches to assess both the succession of phages and bacterial communities on the cheese surface during cheese ripening, and their variations in ready-to-eat cheeses over 4 years of production. They observed a transition of the phage community structure during ripening with a decreased relative abundance of viral species (vOTUs) associated with Lactococcus phages, which were replaced by vOTUs associated with phages infecting ripening bacteria such as Brevibacterium, Glutamicibacter, Pseudoalteromonas and Vibrio. Specifically, the relative abundance of several phages, such as Glutamicibacter phage Montesquieu, Psychrobacter phage d’Alembert and Lactococcus phages belonging to the (Skunavirus genus), KSY1 and P335 groups was positively correlated to the relative abundance of their predicted bacterial hosts.

The work is clearly and accurately presented, well-structured and well-written. The main study claims are very well-justified by the data and analytic methods used. The tables and figures are chosen and designed with relevance and style. Therefore, the overall conclusions and main claims detailed above are clearly substantiated by the evidence presented. They should be considered conclusive and actionable without reservation.

The manuscript cites current and relevant literature and discuss limitations. For instance, the authors point out that the observed positive correlation between a phage and its predicted bacterial host contrasts with the anticipated negative correlation that might have been expected if virulent phages were responsible for eliminating key members of the bacterial community during cheese ripening. The authors conclude with good reason that future investigations at strain level would be highly relevant to better understand the ecological role of phages in cheese rind microbial communities. One limitation of the study is the lack of analysis of the fungal community and its virome. The authors could briefly discuss the relevance of this component of the microbiota for the cheese studied.

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