High Level of Interaction between Phages and Bacteria in an Artisanal Raw Milk Cheese Microbial Community

Queiroz, Luciano Lopes; Lacorte, Gustavo Augusto; Isidorio, William Ricardo; Landgraf, Mariza; Franco, Bernadette Dora Gombossy de Melo; Pinto, Uelinton Manoel; Hoffmann, Christian

doi:10.1128/msystems.00564-22

Cited by 12 publications

(6 citation statements)

References 77 publications

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“…Recent studies of cheese samples using viral metagenomics (24,25) or exploration of cheese microbial metagenomes (30) have revealed that the cheese environment harbours a diverse bacteriophage community whose targets go beyond lactic acid starter cultures. The isolation of a few representatives of these non-starter phages (27)(28)(29) suggests that phage activity occurs in this ecosystem, raising the question of their overall impact on microbial successions during the ripening process.…”

Section: Discussionmentioning

confidence: 99%

“…Consequently, the most studied dairy phages are Lactococcus , Streptococcus , Lactobacillus and Leuconostoc phages, infecting the main starter cultures (22). Viral metagenomics has been recently employed to characterize the bacteriophage communities in dairy samples, including whey (23) and cheeses (24, 25). These investigations have demonstrated that such viral communities are not restricted to LAB phages, but encompass a diverse array of phages that could potentially also infect non-inoculated and ripening bacteria during cheese production.…”

Section: Introductionmentioning

confidence: 99%

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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

Paillet,

Lamy-Besnier,

Figueroa

et al. 2023

Preprint

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The 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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dynamics of the viral community on the surface of a French smear-ripened cheese during maturation and persistence across production years

Paillet,

Lamy-Besnier,

Figueroa

et al. 2023

Preprint

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“…Backslopping can be considered as a top-down microbiome engineering approach as it allows the selection of communities increasingly adapted to technological pressures (milk, temperature, salt, pH) while assuring desired functions (11) such as acidification. Omics approaches have been used to unravel key features of microbial community dynamics during backslopping, and the consequences for community function (15)(16)(17)(18)(19)(20). Long-term backslopping leads to communities with low species richness and high intraspecies diversity (21,22).…”

Section: Introductionmentioning

confidence: 99%

Serial fermentation in milk generates functionally diverse community lineages with different degrees of structure stabilization

Gapp,

Dijamentiuk,

Mangavel

et al. 2024

Preprint

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Microbial communities offer considerable potential for tackling environmental challenges by improving the functioning of ecosystems. Top-down community engineering is a promising strategy that could be used to obtain communities of desired function. However, the ecological factors that control the balance between community shaping and propagation are not well understood. Dairy backslopping can be used as a model engineering approach to investigate the dynamics of communities during serial propagations. In this study, 26 raw milk samples were used to generate lineages of 6 communities obtained by serial propagation. Bacterial community structures were analyzed by metabarcoding and acidification was recorded by pH monitoring. The results revealed that different types of community lineages could be obtained in terms of taxonomic composition and dynamics. Five lineages reached a repeatable community structure in a few propagation steps, with little variation between the final generations, giving rise to stable acidification kinetics. Moreover, these stabilized communities presented a high inter-lineage variability of community structures as well as diverse acidification properties. Besides, the other lineages were characterized by different levels of dynamics leading to parallel or divergent trajectories. The functional properties and dynamics of the communities were mainly related to the relative abundance and the taxonomic composition of lactic acid bacteria within the communities. These findings highlight that short-term schemes of serial fermentation can produce communities with a wide range of dynamics and that the balance between community shaping and propagation is intimately linked to community structure.

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“…Pingo is a natural starter culture composed of fermented whey from the previous day’s batch, containing lactic acid bacteria (LAB)—such as those from the genera Lactobacillus , Lactococcus , Streptococcus , and others [ 8 ]. The most abundant bacterial species in the pingo from Canastra cheese are Lactococcus lactis , Streptococcus thermophilus , Streptococcus infantarius , Streptococcus salivarius , and Corynebacterium variabile [ 9 ]. Additionally, a portion of the cheese that is grated after the ripening process and known as rala could be considered as a substitute for pingo .…”

Section: Introductionmentioning

confidence: 99%

Unveiling Safety Concerns in Brazilian Artisanal Cheeses: A Call for Enhanced Ripening Protocols and Microbiological Assessments

de Albuquerque,

Campos,

d’Ovidio

et al. 2024

Foods

Self Cite

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Brazilian artisanal cheeses have recently gained significant commercial prominence and consumer favor, primarily due to their distinctive sensory attributes and cultural and historical appeal. Many of these cheeses are made with raw milk and undergo a relatively short ripening period, sometimes ranging from 4 to 8 days, though it is usually shorter than the period stated by law. Moreover, there is insufficient evidence regarding the efficacy of a short ripening period in reducing certain zoonotic foodborne pathogens, such as Brucella spp., Coxiella burnetiid, and Mycobacterium bovis (as part of the Mycobacterium tuberculosis complex). Additionally, a literature analysis revealed that the usual ripening conditions of Brazilian artisanal cheeses made with raw milk may be inefficient in reducing the levels of some hazardous bacterial, including Brucella spp., Listeria monocytogenes, coagulase-positive Staphylococcus, Salmonella, and Coxiella burnetti, to the acceptable limits established by law, thus failing to ensure product safety for all cheese types. Moreover, the assessment of the microbiological safety for this type of cheese should be broader and should also consider zoonotic pathogens commonly found in bovine herds. Finally, a standardized protocol for evaluating the effectiveness of cheese ripening must be established by considering its peculiarities.

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High Level of Interaction between Phages and Bacteria in an Artisanal Raw Milk Cheese Microbial Community

Cited by 12 publications

References 77 publications

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

Serial fermentation in milk generates functionally diverse community lineages with different degrees of structure stabilization

Unveiling Safety Concerns in Brazilian Artisanal Cheeses: A Call for Enhanced Ripening Protocols and Microbiological Assessments

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