Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese

Abstract Background Numerous studies have highlighted the impact of bacterial communities on the quality and safety of raw ewe milk-derived cheeses. Despite reported differences in the microbiota among cheese types and even producers, to the best of our knowledge, no study has comprehensively assess...

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Main Authors: Gorka Santamarina-García, Min Yap, Fiona Crispie, Gustavo Amores, Cathy Lordan, Mailo Virto, Paul D. Cotter
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Microbiome
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Online Access:https://doi.org/10.1186/s40168-024-01980-0
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author Gorka Santamarina-García
Min Yap
Fiona Crispie
Gustavo Amores
Cathy Lordan
Mailo Virto
Paul D. Cotter
author_facet Gorka Santamarina-García
Min Yap
Fiona Crispie
Gustavo Amores
Cathy Lordan
Mailo Virto
Paul D. Cotter
author_sort Gorka Santamarina-García
collection DOAJ
description Abstract Background Numerous studies have highlighted the impact of bacterial communities on the quality and safety of raw ewe milk-derived cheeses. Despite reported differences in the microbiota among cheese types and even producers, to the best of our knowledge, no study has comprehensively assessed all potential microbial sources and their contributions to any raw ewe milk-derived cheese, which could suppose great potential for benefits from research in this area. Here, using the Protected Designation of Origin Idiazabal cheese as an example, the impact of the environment and practices of artisanal dairies (including herd feed, teat skin, dairy surfaces, and ingredients) on the microbiomes of the associated raw milk, whey, and derived cheeses was examined through shotgun metagenomic sequencing. Results The results revealed diverse microbial ecosystems across sample types, comprising more than 1300 bacterial genera and 3400 species. SourceTracker analysis revealed commercial feed and teat skin as major contributors to the raw milk microbiota (45.6% and 33.5%, respectively), being a source of, for example, Lactococcus and Pantoea, along with rennet contributing to the composition of whey and cheese (17.4% and 41.0%, respectively), including taxa such as Streptococcus, Pseudomonas_E or Lactobacillus_H. Functional analysis linked microbial niches to cheese quality- and safety-related metabolic pathways, with brine and food contact surfaces being most relevant, related to genera like Brevibacterium, Methylobacterium, or Halomonas. With respect to the virulome (virulence-associated gene profile), in addition to whey and cheese, commercial feed and grass were the main reservoirs (related to, e.g., Brevibacillus_B or CAG-196). Similarly, grass, teat skin, or rennet were the main contributors of antimicrobial resistance genes (e.g., Bact-11 or Bacteriodes_B). In terms of cheese aroma and texture, apart from the microbiome of the cheese itself, brine, grass, and food contact surfaces were key reservoirs for hydrolase-encoding genes, originating from, for example, Lactococcus, Lactobacillus, Listeria or Chromohalobacter. Furthermore, over 300 metagenomic assembled genomes (MAGs) were generated, including 60 high-quality MAGs, yielding 28 novel putative species from several genera, e.g., Citricoccus, Corynebacterium, or Dietzia. Conclusion This study emphasizes the role of the artisanal dairy environments in determining cheese microbiota and, consequently, quality and safety. Video Abstract
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spelling doaj-art-27d7df8d33ba4bb19bc258d7d10506c72024-12-22T12:36:55ZengBMCMicrobiome2049-26182024-12-0112112310.1186/s40168-024-01980-0Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheeseGorka Santamarina-García0Min Yap1Fiona Crispie2Gustavo Amores3Cathy Lordan4Mailo Virto5Paul D. Cotter6Lactiker Research Group, Department of Biochemistry and Molecular Biology, Faculty of Pharmacy, University of the Basque Country (UPV/EHU)Department of Food Biosciences, Teagasc Food Research Centre, Teagasc-The Irish Agriculture and Food Development Authority, Moorepark, Fermoy, Co.Department of Food Biosciences, Teagasc Food Research Centre, Teagasc-The Irish Agriculture and Food Development Authority, Moorepark, Fermoy, Co.Lactiker Research Group, Department of Biochemistry and Molecular Biology, Faculty of Pharmacy, University of the Basque Country (UPV/EHU)Department of Food Biosciences, Teagasc Food Research Centre, Teagasc-The Irish Agriculture and Food Development Authority, Moorepark, Fermoy, Co.Lactiker Research Group, Department of Biochemistry and Molecular Biology, Faculty of Pharmacy, University of the Basque Country (UPV/EHU)Department of Food Biosciences, Teagasc Food Research Centre, Teagasc-The Irish Agriculture and Food Development Authority, Moorepark, Fermoy, Co.Abstract Background Numerous studies have highlighted the impact of bacterial communities on the quality and safety of raw ewe milk-derived cheeses. Despite reported differences in the microbiota among cheese types and even producers, to the best of our knowledge, no study has comprehensively assessed all potential microbial sources and their contributions to any raw ewe milk-derived cheese, which could suppose great potential for benefits from research in this area. Here, using the Protected Designation of Origin Idiazabal cheese as an example, the impact of the environment and practices of artisanal dairies (including herd feed, teat skin, dairy surfaces, and ingredients) on the microbiomes of the associated raw milk, whey, and derived cheeses was examined through shotgun metagenomic sequencing. Results The results revealed diverse microbial ecosystems across sample types, comprising more than 1300 bacterial genera and 3400 species. SourceTracker analysis revealed commercial feed and teat skin as major contributors to the raw milk microbiota (45.6% and 33.5%, respectively), being a source of, for example, Lactococcus and Pantoea, along with rennet contributing to the composition of whey and cheese (17.4% and 41.0%, respectively), including taxa such as Streptococcus, Pseudomonas_E or Lactobacillus_H. Functional analysis linked microbial niches to cheese quality- and safety-related metabolic pathways, with brine and food contact surfaces being most relevant, related to genera like Brevibacterium, Methylobacterium, or Halomonas. With respect to the virulome (virulence-associated gene profile), in addition to whey and cheese, commercial feed and grass were the main reservoirs (related to, e.g., Brevibacillus_B or CAG-196). Similarly, grass, teat skin, or rennet were the main contributors of antimicrobial resistance genes (e.g., Bact-11 or Bacteriodes_B). In terms of cheese aroma and texture, apart from the microbiome of the cheese itself, brine, grass, and food contact surfaces were key reservoirs for hydrolase-encoding genes, originating from, for example, Lactococcus, Lactobacillus, Listeria or Chromohalobacter. Furthermore, over 300 metagenomic assembled genomes (MAGs) were generated, including 60 high-quality MAGs, yielding 28 novel putative species from several genera, e.g., Citricoccus, Corynebacterium, or Dietzia. Conclusion This study emphasizes the role of the artisanal dairy environments in determining cheese microbiota and, consequently, quality and safety. Video Abstracthttps://doi.org/10.1186/s40168-024-01980-0MetagenomicsShotgun sequencingVirulence factorsAntimicrobial resistance genesHydrolase-encoding genesMetagenome-assembled genomes
spellingShingle Gorka Santamarina-García
Min Yap
Fiona Crispie
Gustavo Amores
Cathy Lordan
Mailo Virto
Paul D. Cotter
Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese
Microbiome
Metagenomics
Shotgun sequencing
Virulence factors
Antimicrobial resistance genes
Hydrolase-encoding genes
Metagenome-assembled genomes
title Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese
title_full Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese
title_fullStr Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese
title_full_unstemmed Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese
title_short Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese
title_sort shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes quality and safety of idiazabal a raw ewe milk pdo cheese
topic Metagenomics
Shotgun sequencing
Virulence factors
Antimicrobial resistance genes
Hydrolase-encoding genes
Metagenome-assembled genomes
url https://doi.org/10.1186/s40168-024-01980-0
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