Comparative analysis of the microbiome composition of artisanal cheeses produced in the Mediterranean area

Submitted: 17 July 2024
Accepted: 9 September 2024
Published: 10 October 2024
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In the PRIMA project ArtiSaneFood, the microbiological parameters of several artisanal cheeses produced in the Mediterranean area have been quantified. In this pilot study, we selected four of these artisanal cheese products from Italy, Portugal, Spain, and Morocco to investigate and compare their microbiomes in terms of taxonomy composition, presence of reads of foodborne pathogens, as well as virulence and antimicrobial resistance genes. Lactococcus, Streptococcus and Lactobacillus were the most represented genera in the Portuguese and Spanish cheeses, Streptococcus in the Italian cheese, and Enterococcus, Klebsiella, Escherichia, and Citrobacter in the Moroccan products. The correlation analysis indicated a negative association between the abundance of some lactic acid bacteria (i.e., Lactococcus, Lactobacillus, Streptococcus, and Leuconostoc) and foodborne pathogenic genera, like Escherichia and Salmonella. The analysis of pathogen abundance, virulence factors, and antimicrobial resistance genes showed a strong clusterization based on the cheese type, confirming that the presence of potential human health risk determinants was higher in the artisanal products derived from unpasteurized milk that underwent spontaneous fermentation.

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Adams MR, Nicolaides L, 1997. Review of the sensitivity of different foodborne pathogens to fermentation. Food Control 8;227-39. DOI: https://doi.org/10.1016/S0956-7135(97)00016-9
Alcock BP, Huynh W, Chalil R, Smith KW, Raphenya AR, Wlodarski MA, Edalatmand A, Petkau A, Syed SA, Tsang KK, Baker SJC, Dave M, Mccarthy MC, Mukiri KM, Nasir JA, Golbon B, Imtiaz H, Jiang X, Kaur K, Kwong M, Liang ZC, Niu KC, Shan P, Yang JYJ, Gray KL, Hoad GR, Jia B, Bhando T, Carfrae LA, Farha MA, French S, Gordzevich R, Rachwalski K, Tu MM, Bordeleau E, Dooley D, Griffiths E, Zubyk HL, Brown ED, Maguire F, Beiko RG, Hsiao WWL, Brinkman FSL, Van Domselaar G, McArthur AG, 2023. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the Comprehensive Antibiotic Resistance Database. Nucleic Acids Research 51:D690-9. DOI: https://doi.org/10.1093/nar/gkac920
Anderson AC, Jonas D, Huber I, Karygianni L, Wölber J, Hellwig E, Arweiler N, Vach K, Wittmer A, Al-Ahmad A, 2016. Enterococcus faecalis from food, clinical specimens, and oral sites: prevalence of virulence factors in association with biofilm formation. Front Microbiol 6:1534. DOI: https://doi.org/10.3389/fmicb.2015.01534
Aquilanti L, Kahraman O, Zannini E, Osimani A, Silvestri G, Ciarrocchi F, Garofalo C, Tekin E, Clementi F, 2012. Response of lactic acid bacteria to milk fortification with dietary zinc salts. Int Dairy J 25:52-9. DOI: https://doi.org/10.1016/j.idairyj.2011.12.006
Azzouz S, Ahadaf S, Zantar S, El Galiou O, Arakrak A, Bakkali M, Laglaoui A, 2024. Analysis of the bacterial diversity in Moroccan Jben cheese using TTGE, DGGE, and 16S rRNA sequencing. World J Microbiol Biotechnol 40:157. DOI: https://doi.org/10.1007/s11274-024-03964-6
Baylis CL, 2009. Raw milk and raw milk cheeses as vehicles for infection by Verocytotoxin‐producing Escherichia coli. Int J Dairy Technol 62:293-307. DOI: https://doi.org/10.1111/j.1471-0307.2009.00504.x
Bray NL, Pimentel H, Melsted P, Pachter L, 2016. Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol 34:525-7. DOI: https://doi.org/10.1038/nbt.3519
Cabezas L, Sánchez I, Poveda JM, Seseña S, Palop MLL, 2007. Comparison of microflora, chemical and sensory characteristics of artisanal Manchego cheeses from two dairies. Food Control 18:11-7. DOI: https://doi.org/10.1016/j.foodcont.2005.07.010
Campagnollo FB, Pedrosa GTS, Kamimura BA, Furtado MM, Baptista RC, Nascimento HM, Alvarenga VO, Magnani M, Sant’Ana AS, 2022. Growth potential of three strains of Listeria monocytogenes and Salmonella enterica in Frescal and semi-hard artisanal Minas microcheeses: Impact of the addition of lactic acid bacteria with antimicrobial activity. LWT 158:113169. DOI: https://doi.org/10.1016/j.lwt.2022.113169
dos Santos RA, Araújo GB, Correia EF, de Souza Costa Sobrinho P, 2022. Minas artisanal cheese as potential source of multidrug-resistant Escherichia coli. Foodborne Pathog Dis 19:316-23. DOI: https://doi.org/10.1089/fpd.2021.0102
EFSA, 2015. Scientific Opinion on the public health risks related to the consumption of raw drinking milk. EFSA J 13:3940. DOI: https://doi.org/10.2903/j.efsa.2015.3940
EFSA, 2023. The European Union one health 2022 zoonoses report. EFSA J 21:e8442. DOI: https://doi.org/10.2903/j.efsa.2023.p211202
Faria AS, Coelho-Fernande S, Santos-Rodrigue G, Fernandes Â, Barros L, Cadavez V, Gonzales-Barron U, 2022. Microbiological quality profile of goat’s raw milk cheese during ripening as affected by its intrinsic properties. 2th International Conference on Simulation and Modelling in the Food and Bio-Industry 2022. Foodsim 46-53.
Gould LH, Mungai E, Barton Behravesh C, 2014. Outbreaks attributed to cheese: differences between outbreaks caused by unpasteurized and pasteurized dairy products, United States, 1998–2011. Foodborne Pathog Dis 11:545-51. DOI: https://doi.org/10.1089/fpd.2013.1650
Hamama A, Bayi M, 1991. Composition and microbiological profile of two Moroccan traditional dairy products: raib and jben. Int J Dairy Technol 44:118-20. DOI: https://doi.org/10.1111/j.1471-0307.1991.tb01921.x
Handelsman J, 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669-85. DOI: https://doi.org/10.1128/MMBR.68.4.669-685.2004
Hartantyo SHP, Chau ML, Koh TH, Yap M, Yi T, Cao DYH, Gutiérrez RA, Ng LC, 2020. Foodborne Klebsiella pneumoniae: virulence potential, antibiotic resistance, and risks to food safety. J Food Prot 83:1096-103. DOI: https://doi.org/10.4315/JFP-19-520
Indio V, Olivieri C, Lucchi A, Savini F, Gonzales-Barron U, Skandamis P, Achemchem F, Manfreda G, Serraino A, De Cesare A, 2024. Shotgun metagenomic investigation of foodborne pathogens and antimicrobial resistance genes in artisanal fermented meat products from the Mediterranean area. Ital J Food Safety 2024. doi: 10.4081/ijfs.2024.12210. DOI: https://doi.org/10.4081/ijfs.2024.12210
Keegan KP, Glass EM, Meyer F, 2016. MG-RAST, a metagenomics service for analysis of microbial community structure and function. In: Martin F, Uroz S, eds. Microbial environmental genomics (MEG). Methods in molecular biology, vol 1399. Humana Press, New York, NY, USA; pp. 207-33). DOI: https://doi.org/10.1007/978-1-4939-3369-3_13
Koutsoumanis K, Allende A, Alvarez‐Ordóñez A, Bolton D, Bover‐Cid S, Chemaly M, Davies R, De Cesare A, Hilbert F, Lindqvist R, Nauta M, Peixe L, Ru G, Simmons M, Skandamis P, Suffredini E, Jenkins C, Malorny B, Ribeiro Duarte AS, Torpdahl M, da Silva Felício MT, Guerra B, Rossi M, Herman L, 2019. Whole genome sequencing and metagenomics for outbreak investigation, source attribution and risk assessment of food‐borne microorganisms. EFSA J 17:e05898. DOI: https://doi.org/10.2903/j.efsa.2019.5898
Leech J, Cabrera-Rubio R, Walsh AM, Macori G, Walsh CJ, Barton W, Finnegan L, Crispie F, O’Sullivan O, Claesson MJ, Cotter PD, 2020. Fermented-food metagenomics reveals substrate-associated differences in taxonomy and health-associated and antibiotic resistance determinants. MSystems 5:e00522-20. DOI: https://doi.org/10.1128/mSystems.00522-20
Liu B, Zheng D, Zhou S, Chen L, Yang J, 2022. VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res 50:D912-7. DOI: https://doi.org/10.1093/nar/gkab1107
Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J, 2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18. DOI: https://doi.org/10.1186/2047-217X-1-18
Martin NH, Trmčić A, Hsieh TH, Boor KJ, Wiedmann M, 2016. The evolving role of coliforms as indicators of unhygienic processing conditions in dairy foods. Front Microbiol 7:1549. DOI: https://doi.org/10.3389/fmicb.2016.01549
Pasquali F, Valero A, Possas A, Lucchi A, Crippa C, Gambi L, Manfreda G, De Cesare A, 2022. Occurrence of foodborne pathogens in Italian soft artisanal cheeses displaying different intra- and inter-batch variability of physicochemical and microbiological parameters. Front Microbiol 13:959648. DOI: https://doi.org/10.3389/fmicb.2022.959648
Pérez-Rodríguez F, Mercanoglu Taban B, 2019. A state-of-art review on multi-drug resistant pathogens in foods of animal origin: risk factors and mitigation strategies. Front Microbiol 10:2091. DOI: https://doi.org/10.3389/fmicb.2019.02091
Possas A, Hernández M, Esteban-Carbonero Ó, Valero A, Rodríguez-Lázaro D, 2022. Listeria monocytogenes survives better at lower storage temperatures in regular and low-salt soft and cured cheeses. Food Microbiol 104:103979. DOI: https://doi.org/10.1016/j.fm.2022.103979
Quintana ÁR, Perea JM, Palop ML, Garzón A, Arias R, 2020. Influence of environmental and productive factors on the biodiversity of lactic acid bacteria population from sheep milk. Animals 10:2180. DOI: https://doi.org/10.3390/ani10112180
Rangel-Ortega SdC, Campos-Múzquiz LG, Charles-Rodriguez AV, Chávez-Gonzaléz ML, Palomo-Ligas L, Contreras-Esquivel JC, Solanilla-Duque JF, Flores-Gallegos AC, Rodríguez-Herrera R, 2023. Biological control of pathogens in artisanal cheeses. Int Dairy J 140:105612. DOI: https://doi.org/10.1016/j.idairyj.2023.105612
Siroli L, Patrignani F, D’Alessandro M, Salvetti E, Torriani S, Lanciotti R, 2020. Suitability of the Nisin Z-producer Lactococcus lactis subsp. lactis CBM 21 to be used as an adjunct culture for Squacquerone cheese production. Animals 10:782. DOI: https://doi.org/10.3390/ani10050782
Thierry A, Valence F, Deutsch SM, Even S, Falentin H, Le Loir Y, Jan G, Gagnaire V, 2015. Strain-to-strain differences within lactic and propionic acid bacteria species strongly impact the properties of cheese - a review. Dairy Sci Technol 95:895-918. DOI: https://doi.org/10.1007/s13594-015-0267-9
Ünlü T, Koluman A, Burkan ZT, Tezel A, Akçelik EN, Çalim HD, Ata Z, 2011. Incidence and antibiotic resistance of Escherichia coli isolated from different kinds of cheese. J Food Safety 31:54-60. DOI: https://doi.org/10.1111/j.1745-4565.2010.00266.x
Walsh AM, Macori G, Kilcawley KN, Cotter PD, 2020. Meta-analysis of cheese microbiomes highlights contributions to multiple aspects of quality. Nat Food 1:500-10. DOI: https://doi.org/10.1038/s43016-020-0129-3
Yoon Y, Lee S, Choi KH, 2016. Microbial benefits and risks of raw milk cheese. Food Control 63:201-15. DOI: https://doi.org/10.1016/j.foodcont.2015.11.013

How to Cite

1.
Indio V, Gonzales-Barron U, Oliveri C, Lucchi A, Valero A, Achemchem F, Manfreda G, Savini F, Serraino A, De Cesare A. Comparative analysis of the microbiome composition of artisanal cheeses produced in the Mediterranean area. Ital J Food Safety [Internet]. 2024 Oct. 10 [cited 2024 Dec. 19];13(4). Available from: https://www.pagepressjournals.org/ijfs/article/view/12818