Review on the NGS-based studies of microbiotas of artisanal and regional kinds of cheese with potential as functional foods: composition and functional analysis

Figures & data

Table 1. Examples of amplicon-based metagenomic studies of different kinds of cheeses worldwide

Examples	Platforms	References
Studies performed on platforms with short reads
Bulgarian Krokmach cheese	Illumina	[45]
Bulgarian Green cheese	Illumina	[112]
Colombian Paipa cheese	Illumina	[113]
Cyprian Halloumi cheese	Illumina	[114]
Greek Halitziacheeses	Illumina	[115]
Cheese from the Uighur Autonomy Region in China	Illumina	[116]
Italian Buffalo Mozzarella cheese	Illumina, Ion Torrent	[117,118]
Turkish Tulum cheese	Illumina, Ion Torrent	[119,120]
French Tomme d’Orchides cheese	Illumina	[121]
Brine-salted continental-type cheese	Roche 454	[122]
Irish artisanal cheeses	Roche 454	[123]
Mexican Bola de Ocosingo cheese	Roche 454	[124]
Mexican artisanal Adobera cheese from Los Altos de Jalisco	Ion Torrent	[120]
Studies performed on platforms with short reads
Russian local Buryat cheeses	PacBio	[125]
Austrian Vorarlberger Bergkäse	PacBio	[21]
Kazakhstan’s traditional artisanal cheeses	PacBio	[126]
Belgian artisanal cheeses	PacBio	[126]
Russian artisanal cheeses from Kalmykia	PacBio	[126]
Slovak traditional ewe’s milk cheese	Oxford Nanopores	[127]
Swiss Brie cheese	Oxford Nanopores	[128]
Swiss Camambert cheese	Oxford Nanopores	[128]

Table 2. Examples of whole-metagenome sequencing studies of different kinds of cheeses worldwide

Examples	Platforms	References
Studies performed on platforms with short reads
Comparative study of eight different cheeses from China, Italy, and Greece	Illumina	[129]
Halitzia cheese from Cyprus	Illumina	[130]
Montenegrin brine cheeses	Illumina	[131]
Greek Kasseri cheese	Illumina	[132]
Greek Kopanisti cheese	Illumina	[133]
Argentinean artisanal cheeses	Ion Torrent	[134]
Artisanal Flemish cheese in Belgium	Ion Torrent	[135]
Studies performed on platforms with short reads
Experimentally produced cheese obtained from dairy ewes fed a dietary hemp seed supplementation	Oxford Nanopores	[136]

Table 3. Comparison between amplicon and shotgun sequencing

	Amplicon sequencing	Shotgun sequencing
Advantages	- Small sample volumes	- Very high resolution
	- The results are associated with a single kingdom	- Sequencing broad regions of the genome
	- Cheap
Disadvantages	- Smaller taxonomic resolution	- Results for a single kingdom are harder to distinguish
	- Variations in the number of amplicons	- Need of larger sample volumes
		- Expensive

Dimov SG. The unusual microbiota of the traditional Bulgarian dairy product Krokmach – a pilot metagenomics study. Int J Dairy Tech. 2022;75(1):139–149. doi: 10.1111/1471-0307.12809.

 Google Scholar

Dimov SG, Gyurova A, Zagorchev L, et al. NGS-Based metagenomic study of four traditional Bulgarian green cheeses from Tcherni Vit. LWT. 2021;152:112278. doi: 10.1016/j.lwt.2021.112278.

 Google Scholar

Castellanos-Rozo J, Pérez Pulido R, Grande MJ, et al. Analysis of the bacterial diversity of paipa cheese (a traditional raw cow’s milk cheese from Colombia) by high-throughput sequencing. Microorganisms. 2020;8(2):218. doi: 10.3390/microorganisms8020218.

 PubMedGoogle Scholar

Kamilari E, Anagnostopoulos DA, Papademas P, et al. Characterizing halloumi cheese’s bacterial communities through metagenomic analysis. LWT. 2020;126:109298. doi: 10.1016/j.lwt.2020.109298.

 Google Scholar

Papademas P, Aspri M, Mariou M, et al. Conventional and omics approaches shed light on Halitzia cheese, a long-forgotten white-brined cheese from Cyprus. Int Dairy J. 2019;98:72–83. doi: 10.1016/j.idairyj.2019.06.010.

 Google Scholar

Zheng X, Liu F, Shi X, et al. Dynamic correlations between microbiota succession and flavor development involved in the ripening of Kazak artisanal cheese. Food Res Int. 2018;105:733–742. doi: 10.1016/j.foodres.2017.12.007.

 PubMedGoogle Scholar

Marino M, Dubsky de Wittenau G, Saccà E, et al. Metagenomic profiles of different types of Italian high-moisture Mozzarella cheese. Food Microbiol. 2019;79:123–131. doi: 10.1016/j.fm.2018.12.007.

 PubMedGoogle Scholar

Ribani A, Schiavo G, Utzeri VJ, et al. Application of next generation semiconductor based sequencing for species identification in dairy products. Food Chem. 2018;246:90–98. doi: 10.1016/j.foodchem.2017.11.006.

 PubMed Web of Science ®Google Scholar

Gezginc Y, Karabekmez-Erdem T, Tatar HD, et al. Metagenomics and volatile profile of Turkish artisanal Tulum cheese microbiota. Food Biosci. 2022;45:101497. doi: 10.1016/j.fbio.2021.101497.

 Google Scholar

Güley Z, Fallico V, Cabrera-Rubio R, et al. Diversity of the microbiota of traditional izmir tulum and izmir brined tulum cheeses and selection of potential probiotics. Foods. 2023;12(18):3482. doi: 10.3390/foods12183482.

 PubMedGoogle Scholar

Ceugniez A, Taminiau B, Coucheney F, et al. Fungal diversity of “Tomme d’Orchies” cheese during the ripening process as revealed by a metagenomic study. Int J Food Microbiol. 2017;258:89–93. doi: 10.1016/j.ijfoodmicro.2017.07.015.

 PubMedGoogle Scholar

O’Sullivan Daniel J, Cotter Paul D, O’Sullivan O, et al. Temporal and spatial differences in microbial composition during the manufacture of a continental-type cheese. Appl Environ Microbiol. 2015;81(7):2525–2533. doi: 10.1128/AEM.04054-14.

 PubMedGoogle Scholar

Quigley L, O’Sullivan O, Beresford Tom P, et al. High-throughput sequencing for detection of subpopulations of bacteria not previously associated with artisanal cheeses. Appl Environ Microbiol. 2012;78(16):5717–5723. doi: 10.1128/AEM.00918-12.

 PubMed Web of Science ®Google Scholar

Aldrete-Tapia A, Escobar-Ramírez CM, Tamplin ML, et al. Characterization of bacterial communities in Mexican artisanal raw milk “Bola de Ocosingo” cheese by high-throughput sequencing. Front Microbiol. 2018;9:2598. doi: 10.3389/fmicb.2018.02598.

 PubMedGoogle Scholar

Jin H, Mo L, Pan L, et al. Using PacBio sequencing to investigate the bacterial microbiota of traditional Buryatian cottage cheese and comparison with Italian and Kazakhstan artisanal cheeses. J Dairy Sci. 2018;101(8):6885–6896. doi: 10.3168/jds.2018-14403.

 PubMedGoogle Scholar

Quijada NM, Schmitz-Esser S, Zwirzitz B, et al. Austrian raw-milk hard-cheese ripening involves successional dynamics of non-inoculated bacteria and fungi. Foods. 2020;9(12):1851. doi: 10.3390/foods9121851.

 PubMedGoogle Scholar

Li J, Zheng Y, Xu H, et al. Bacterial microbiota of Kazakhstan cheese revealed by single molecule real time (SMRT) sequencing and its comparison with Belgian, Kalmykian and Italian artisanal cheeses. BMC Microbiol. 2017;17(1):13. doi: 10.1186/s12866-016-0911-4.

 PubMedGoogle Scholar

Planý M, Sitarčík J, Pavlović J, et al. Evaluation of bacterial consortia associated with dairy fermentation by ribosomal RNA (rrn) operon metabarcoding strategy using MinION device. Food Biosci. 2023;51:102308. doi: 10.1016/j.fbio.2022.102308.

 Google Scholar

Catozzi C, Ceciliani F, Lecchi C, et al. Short communication: milkmicrobiota profiling on water buffalo with full-length 16S rRNA using nanopore sequencing. J Dairy Sci. 2020;103(3):2693–2700. doi: 10.3168/jds.2019-17359.

 PubMedGoogle Scholar

Yang C, You L, Kwok L-Y, et al. Strain-level multiomics analysis reveals significant variation in cheeses from different regions. LWT. 2021;151:112043. doi: 10.1016/j.lwt.2021.112043.

 Web of Science ®Google Scholar

Papadimitriou K, Venieraki A, Tsigkrimani M, et al. Whole-genome sequence data of the proteolytic and bacteriocin producing strain Enterococcus faecalis PK23 isolated from the traditional Halitzia cheese produced in Cyprus. Data Brief. 2021;38:107437. doi: 10.1016/j.dib.2021.107437.

 PubMedGoogle Scholar

Ruppitsch W, Nisic A, Hyden P, et al. Genetic diversity of Leuconostoc mesenteroides isolates from traditional montenegrin brine cheese. Microorganisms. 2021;9(8):1612. doi: 10.3390/microorganisms9081612.

 PubMedGoogle Scholar

Alexandraki V, Kazou M, Pot B, et al. Whole-genome sequence data and analysis of Lactobacillus delbrueckii subsp. lactis ACA-DC 178 isolated from Greek kasseri cheese. Data Brief. 2019;25:104282. doi: 10.1016/j.dib.2019.104282.

 PubMedGoogle Scholar

Kazou M, Alexandraki V, Pot B, et al. Whole-genome sequence of the cheese isolate lactobacillus rennini ACA-DC 565. Genome Announc. 2017;5(5):e01579-16. doi: 10.1128/genomea.01579-16.

 PubMedGoogle Scholar

Suárez N, Weckx S, Minahk C, et al. Metagenomics-based approach for studying and selecting bioprotective strains from the bacterial community of artisanal cheeses. Int J Food Microbiol. 2020;335:108894. doi: 10.1016/j.ijfoodmicro.2020.108894.

 PubMed Web of Science ®Google Scholar

Vermote L, Verce M, De Vuyst L, et al. Amplicon and shotgun metagenomic sequencing indicates that microbial ecosystems present in cheese brines reflect environmental inoculation during the cheese production process. Int Dairy J. 2018;87:44–53. doi: 10.1016/j.idairyj.2018.07.010.

 Google Scholar

Ianni A, Di Domenico M, Bennato F, et al. Metagenomic and volatile profiles of ripened cheese obtained from dairy ewes fed a dietary hemp seed supplementation. J Dairy Sci. 2020;103(7):5882–5892. doi: 10.3168/jds.2019-17954.

 PubMedGoogle Scholar

Data availability statement

Data sharing does not apply to this article as no new data were created or analyzed in this study.