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Molecular Identification and Enzymatic Characterization of Fungi Isolated During Beef Aging.

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Τίτλος: Molecular Identification and Enzymatic Characterization of Fungi Isolated During Beef Aging.
Συγγραφείς: Tomasello F; Food Safety and Functionality, IRTA, Monells, Spain., Torrents-Masoliver B; Food Safety and Functionality, IRTA, Monells, Spain., Martín B; Food Safety and Functionality, IRTA, Monells, Spain., Jofré A; Food Safety and Functionality, IRTA, Monells, Spain., Bover-Cid S; Food Safety and Functionality, IRTA, Monells, Spain., Font-I-Furnols M; Food Quality and Technology, IRTA, Monells, Spain., Panella-Riera N; Food Quality and Technology, IRTA, Monells, Spain.
Πηγή: Journal of food science [J Food Sci] 2026 Oct; Vol. 91 (10), pp. e71445.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Wiley on behalf of the Institute of Food Technologists Country of Publication: United States NLM ID: 0014052 Publication Model: Print Cited Medium: Internet ISSN: 1750-3841 (Electronic) Linking ISSN: 00221147 NLM ISO Abbreviation: J Food Sci Subsets: MEDLINE
Imprint Name(s): Publication: Malden, Mass. : Wiley on behalf of the Institute of Food Technologists
Original Publication: Champaign, Ill. Institute of Food Technologists
Ιατρικοί όροι (MeSH): Fungi*/isolation & purification , Fungi*/enzymology , Fungi*/classification , Fungi*/genetics , Red Meat*/microbiology , Red Meat*/analysis, Penicillium/isolation & purification ; Food Handling/methods ; Animals ; Cattle ; Food Microbiology ; Proteolysis
Περίληψη: Dry-aged beef is valued for its distinctive flavor and tenderness, but the fungal communities associated with the product and its aging environments remain insufficiently characterized. This study characterized the culturable fungal community of dry- and wet-aged beef from Albera and Bruna dels Pirineus cattle, as well as the aging chambers where the beef was produced, and assessed the proteolytic and lipolytic potential of the isolated fungi. Meat samples and chamber air were analyzed using culturomics and ITS sequencing. Among 291 fungal isolates, yeasts predominated in meat samples, with Candida, Yarrowia, and Debaryomyces as the main genera, whereas molds were more frequent in chamber samples, especially Penicillium and Cladosporium. Dry-aged meat exhibited a higher diversity of fungal genera and species than wet-aged meat, and some taxa detected in meat were also present in the corresponding aging environments, suggesting a possible environmental contribution. Enzymatic assays showed that many molds and yeasts displayed proteolytic and lipolytic activity, with Yarrowia spp. and Penicillium spp. showing notable activity. However, these assays were performed in vitro and should be interpreted as indicating enzymatic potential rather than direct activity in meat. Although potentially mycotoxigenic genera such as Aspergillus, Cladosporium, and Penicillium were detected, no mycotoxin analyses were performed. Accordingly, no conclusions can be drawn regarding toxin production, but their presence underscores the need for careful control of aging conditions. Overall, the study expands the current knowledge of culturable fungi associated with beef aging systems and provides a basis for future work on the technological and safety relevance of the identified isolates.
(© 2026 Institute of Food Technologists.)
References: Abad, A., J. Victoria Fernández‐Molina, J. Bikandi, et al. 2010. “What Makes Aspergillus fumigatus a Successful Pathogen? Genes and Molecules Involved in Invasive Aspergillosis.” Revista Iberoamericana de Micología 27: 155–182. https://doi.org/10.1016/j.riam.2010.10.003.
Abdel‐Sater, M. A., F. A. Al‐Sharjabi, and E. S. Al‐Ashwal. 2017. “Mycological and Enzymatic Studies on Fresh Beef Meat Sold in Taiz City, Yemen.” European Journal of Biological Research 7: 337–347. https://doi.org/10.5281/zenodo.1037238.
Andersen, B., J. Smedsgaard, and J. C. Frisvad. 2004. “Penicillium expansum: Consistent Production of Patulin, Chaetoglobosins, and Other Secondary Metabolites in Culture and Their Natural Occurrence in Fruit Products.” Journal of Agricultural and Food Chemistry 52: 2421–2428. https://doi.org/10.1021/jf035406k.
Bäumlisberger, M., U. Moellecken, H. König, and H. Claus. 2015. “The Potential of the Yeast Debaryomyces hansenii H525 to Degrade Biogenic Amines in Food.” Microorganisms 3: 839–850. https://doi.org/10.3390/microorganisms3040839.
Berger, J., Y. H. B. Kim, J. F. Legako, et al. 2018. “Dry‐Aging Improves Meat Quality Attributes of Grass‐Fed Beef Loins.” Meat Science 145: 285–291. https://doi.org/10.1016/j.meatsci.2018.07.004.
Beriain, M. J., M. Sanchez, and T. R. Carr. 2009. “A Comparison of Consumer Sensory Acceptance, Purchase Intention, and Willingness to Pay for High Quality United States and Spanish Beef Under Different Information Scenarios.” Journal of Animal Science 87: 3392–3402. https://doi.org/10.2527/jas.2008‐1611.
Bover‐Cid, S., A. Jofré, A. Possas, et al. 2022. “Assessing the Microbiological Safety of Beef Ageing Process: Impact of Temperature and Relative Humidity Conditions.” Paper presented at the 27th International ICFMH Conference FoodMicro2022, Athens, Greece.
Brooks, F. T., and C. G. Hansford. 1923. “Mould Growths Upon Cold‐Store Meat.” Transactions of the British Mycological Society 8: 113–142. https://doi.org/10.1016/S0007‐1536(23)80020‐1.
Capouya, R., T. Mitchell, D. I. Clark, D. L. Clark, and P. Bass. 2020. “A Survey of Microbial Communities on Dry‐Aged Beef in Commercial Meat Processing Facilities.” Meat and Muscle Biology 4: 1–11. https://doi.org/10.22175/mmb.10373.
Cheng, Y., X. Yin, L. Xu, et al. 2023. “Correlation Analysis on the Quality Indicators of Intensified Dry‐Aged Beef and Microbial Succession During Fermentation.” Food Bioscience 56: 103439. https://doi.org/10.1016/j.fbio.2023.103439.
Coton, E., M. Dubée, A. Pawtowski, C. Denoyelle, and J. Mounier. 2024. “Microbiota Associated With Commercial Dry‐Aged Beef in France.” Food Research International 181: 114118. https://doi.org/10.1016/j.foodres.2024.114118.
Dashdorj, D., T. Amna, and I. Hwang. 2015. “Influence of Specific Taste‐Active Components on Meat Flavor as Affected by Intrinsic and Extrinsic Factors: An Overview.” European Food Research and Technology 241: 157–171. https://doi.org/10.1007/s00217‐015‐2449‐3.
Dashdorj, D., V. K. Tripathi, S. Cho, Y. Kim, and I. Hwang. 2016. “Dry Aging of Beef; Review.” Journal of Animal Science and Technology 58: 20. https://doi.org/10.1186/s40781‐016‐01019.
DeGeer, S. L., M. C. Hunt, C. L. Bratcher, B. A. Crozier‐Dodson, D. E. Johnson, and J. F. Stika. 2009. “Effects of Dry Aging of Bone‐In and Boneless Strip Loins Using Two Aging Processes for Two Aging Times.” Meat Science 83: 768–774. https://doi.org/10.1016/j.meatsci.2009.08.017.
EFSA Panel on Biological Hazards (BIOHAZ), K. Koutsoumanis, A. Allende, et al. 2023. “Microbiological Safety of Aged Meat.” EFSA Journal 21: e07745. https://doi.org/10.2903/j.efsa.2023.7745.
Endo, A., R. Koizumi, Y. Nakazawa, et al. 2021. “Characterization of the Microbiota and Chemical Properties of Pork Loins During Dry Aging.” MicrobiologyOpen 10: e1157. https://doi.org/10.1002/mbo3.1157.
European Commission. 2024. Commission Delegated Regulation (EU) 2024/1141 of 14 December 2023 Amending Annexes II and III to Regulation (EC) No 853/2004 of the European Parliament and of the Council as Regards Specific Hygiene Requirements for Certain Meat, Fishery Products, Dairy Products and Eggs.
European Parliament and the Council of the European Union. 2002. Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 Laying Down the General Principles and Requirements of Food Law, Establishing the European Food Safety Authority and Laying Down Procedures in Matters of Food Safety.
Gowda, T. K. G. M., L. De Zutter, G. Van Royen, and I. Van Damme. 2022. “Exploring the Microbiological Quality and Safety of Dry‐Aged Beef: A Cross‐Sectional Study of Loin Surfaces During Ripening and Dry‐Aged Beef Steaks From Commercial Meat Companies in Belgium.” Food Microbiology 102: 103919. https://doi.org/10.1016/j.fm.2021.103919.
International Organization for Standardization (ISO). 2008. ISO 21527‐1:2008—Microbiology of Food and Animal feeding Stuffs—Horizontal Method for the Enumeration of Yeasts and Moulds—Part 1: Colony Count Technique in Products with Water Activity Greater Than 0.95. ISO. https://www.iso.org/standard/38275.html.
Jaeger, K.‐E., and F. Kovacic. 2014. “Determination of Lipolytic Enzyme Activities.” In Pseudomonas Methods and Protocols, edited by A. Filloux and J.‐L. Ramos, 111–134. Springer. https://doi.org/10.1007/978‐1‐4939‐0473‐0_12.
Jaworska, D., J. Pawłowska, E. Kostyra, et al. 2025. “Dry‐Aged Beef Quality With the Addition of Mucor flavus—Sensory, Chemosensory and Fatty Acid Analysis.” Meat Science 220: 109691. https://doi.org/10.1016/j.meatsci.2024.109691.
Jiang, T., J. R. Busboom, M. L. Nelson, et al. 2010. “The Influence of Forage Diets and Aging on Beef Palatability.” Meat Science 86: 642–650. https://doi.org/10.1016/j.meatsci.2010.05.016.
Keller, N. P., and T. H. Adams. 1995. “Analysis of a Mycotoxin Gene Cluster in Aspergillus nidulans.” SAAS Bulletin of Biochemistry and Biotechnology 8: 14–21.
Khazzar, S., S. Segato, G. Riuzzi, et al. 2023. “Influence of Ageing Time and Method on Beef Quality and Safety.” Foods 12: 3250. https://doi.org/10.3390/foods12173250.
Kim, J.‐H., J.‐H. Kim, D.‐K. Yoon, D.‐S. Ji, H.‐J. Jang, and C.‐H. Lee. 2018. “A Comparison of Dry and Wet Aging on Physicochemical and Sensory Characteristics of Pork Loin With Two Aging Times.” Food Science and Biotechnology 27: 1551–1559. https://doi.org/10.1007/s10068‐018‐0418‐x.
Kotula, A. W., S. G. Campano, and D. M. Kinsman. 1982. “Proteolytic and Lipolytic Activity of Molds Isolated From Aged Beef.” Journal of Food Protection 45: 1242–1245. https://doi.org/10.4315/0362‐028X‐45.13.1242.
Lancaster, J. M., J. H. Smart, J. Van Buren, et al. 2022. “Assessment of Dry‐Aged Beef From Commercial Aging Locations Across the United States.” International Journal of Gastronomy and Food Science 27: 100466. https://doi.org/10.1016/j.ijgfs.2022.100466.
Lee, Y. E., H. J. Lee, C. H. Kim, S. Ryu, Y. Kim, and C. Jo. 2022. “Effect of Penicillium candidum and Penicillium nalgiovense and Their Combination on the Physicochemical and Sensory Quality of Dry‐Aged Beef.” Food Microbiology 107: 104083. https://doi.org/10.1016/j.fm.2022.104083.
Li, X.‐A., B. Kong, R. Wen, H. Wang, M. Li, and Q. Chen. 2022. “Flavour Compensation Role of Yeast Strains in Reduced‐Salt Dry Sausages: Taste and Odour Profiles.” Foods 11: 650. https://doi.org/10.3390/foods11050650.
Liu, Y., X. Gao, M. Zang, et al. 2025. “Insights Into Microbial Community and Its Enzymatic Profiles in Commercial Dry‐aged Beef.” Foods 14: 529. https://doi.org/10.3390/foods14030529.
Liu, Y., D. Sun, A. Peng, et al. 2024. “Hydrolysis of Beef Sarcoplasmic Protein by Dry‐Aged Beef‐Isolated Penicillium oxalicum and Its Associated Metabolic Pathways.” Foods 13: 1038. https://doi.org/10.3390/foods13071038.
Liu, M. M., X. M. Zhao, J. Bai, et al. 2026. “Taxogenomic Reclassification of Candida and Related Genera in Saccharomycotina.” Fungal Diversity 136: 136006. https://doi.org/10.65390/fdiv.2026.136006.
Martín, A., M. A. Asensio, M. E. Bermúdez, M. G. Córdoba, E. Aranda, and J. J. Córdoba. 2002. “Proteolytic Activity of Penicillium chrysogenum and Debaryomyces hansenii During Controlled Ripening of Pork Loins.” Meat Science 62: 129–137. https://doi.org/10.1016/S0309‐1740(01)00238‐8.
Martinez, S. 2010. Local Food Systems; Concepts, Impacts, and Issues. DIANE Publishing.
Martorell, P., M. Fernandezespinar, and A. Querol. 2005. “Sequence‐Based Identification of Species Belonging to the Genus Debaryomyces.” FEMS Yeast Research 5: 1157–1165. https://doi.org/10.1016/j.femsyr.2005.05.002.
Meat & Livestock Australia (MLA). 2019. Guidelines for the Safe Production of Dry Aged Meat. MLA.
Mikami, N., T. Toyotome, M. Takaya, and K. Tamura. 2022. “Direct Rub Inoculation of Fungal Flora Changes Fatty Acid Composition and Volatile Flavors in Dry‐Aged Beef: A Preliminary Study.” Animals 12: 1391. https://doi.org/10.3390/ani12111391.
Mikami, N., T. Toyotome, Y. Yamashiro, et al. 2021. “Dry‐Aged Beef Manufactured in Japan: Microbiota Identification and Their Effects on Product Characteristics.” Food Research International 140: 110020. https://doi.org/10.1016/j.foodres.2020.110020.
Nielsen, D. S., T. Jacobsen, L. Jespersen, A. G. Koch, and N. Arneborg. 2008. “Occurrence and Growth of Yeasts in Processed Meat Products—Implications for Potential Spoilage.” Meat Science 80: 919–926. https://doi.org/10.1016/j.meatsci.2008.04.011.
Oh, H., H. J. Lee, J. Lee, C. Jo, and Y. Yoon. 2019. “Identification of Microorganisms Associated With the Quality Improvement of Dry‐Aged Beef Through Microbiome Analysis and DNA Sequencing, and Evaluation of Their Effects on Beef Quality.” Journal of Food Science 84: 2944–2954. https://doi.org/10.1111/1750‐3841.14813.
Panella‐Riera, N., R. Delpiazzo, M. Font‐i‐Furnols, and M. Gil. 2021. “Revalorización de la carne bovina mediante la maduración.” TecnoCarne 00: 42–47.
Panella‐Riera, N., A. Possas, A. Jofré, M. Albano, J. Comaposada, and S. Bover‐Cid. 2021. “Assessment of the Microbiological Safety Associated With the Dynamics of the Meat Surface, Aw, pH and Temperature During Beef Dry Ageing Process.” Poster presented at 67th International Congress of Meat Science and Technology, Kraków, Poland, August 23–27.
Panella‐Riera, N., S. Scappini, M. Font i Furnols, and M. Gil. 2019. “Maduración de carne de bovino en seco y en bolsa tublin hasta 28 y 45 días.” Presented at the AIDA‐XVIII Jornadas sobre Producción Animal, Zaragoza, Spain.
Panella‐Riera, N., M. Vitale, M. Gil, and M. A. Oliver. 2016. “Preliminary Study on the Meat Quality of Albera Bulls, an Endangered Cattle Breed From the Pyrenees.” Presented at the EAAP Annual Meeting, Unpublished, Belfast, UK. https://doi.org/10.13140/RG.2.2.27827.43049.
Panella‐Riera, N., C. Zomeño, G. Martínez, M. Gispert, M. Gil, and M. Font‐i‐Furnols. 2022. “Sensory and Instrumental Characterization of Dry‐aged Loins of Bruna d'Andorra Breed.” Presented at the EAAP Annual Meeting.
Park, B., H. I. Yong, J. Choe, and C. Jo. 2018. “Utilization of the Crust From Dry‐Aged Beef to Enhance Flavor of Beef Patties.” Food Science of Animal Resources 38: 1019–1028. https://doi.org/10.5851/kosfa.2018.e35.
Perea‐Sanz, L., D. Peris, C. Belloch, and M. Flores. 2019. “Debaryomyces hansenii Metabolism of Sulfur Amino Acids as Precursors of Volatile Sulfur Compounds of Interest in Meat Products.” Journal of Agricultural and Food Chemistry 67: 9335–9343. https://doi.org/10.1021/acs.jafc.9b03361.
Pérez, I., and K. C. S. Espinosa. 2019. “Physiological Aspects of the Cladosporium Genus From the Perspective of Its Pathogenic, Phytopathogenic and Biodeteriorant Attributes.” Revista Cubana de Ciencias Biológicas 1: 1–10.
Piontek, M., K. Łuszczyńska, and H. Lechów. 2016. “Occurrence of the Toxin‐Producing Aspergillus versicolor Tiraboschi in Residential Buildings.” International Journal of Environmental Research and Public Health 13: 862. https://doi.org/10.3390/ijerph13090862.
PrimeSafe. 2020. Ageing of Beef PrimeSafe Technical Guideline. https://www.primesafe.vic.gov.au/resources/ageing‐beef/.
Przybylski, W., D. Jaworska, M. Płecha, et al. 2023. “Fungal Biostarter Effect on the Quality of Dry‐Aged Beef.” Foods 12: 1330. https://doi.org/10.3390/foods12061330.
Resconi, V. C., M. M. Campo, M. Font‐i‐Furnols, F. Montossi, and C. Sañudo. 2010. “Sensory Quality of Beef From Different Finishing Diets.” Meat Science 86: 865–869. https://doi.org/10.1016/j.meatsci.2010.07.012.
Rezende‐de‐Souza, J. H., F. A. B. Cardello, A. P. M. de Paula, F. A. Ribeiro, C. R. Calkins, and S. B. Pflanzer. 2021. “Profile of Producers and Production of Dry‐Aged Beef in Brazil.” Foods 10: 2447. https://doi.org/10.3390/foods10102447.
Ryu, S., M. R. Park, B. E. Maburutse, et al. 2018. “Diversity and Characteristics of the Meat Microbiological Community on Dry Aged Beef.” Journal of Microbiology and Biotechnology 28: 105–108. https://doi.org/10.4014/jmb.1708.08065.
Ryu, S., M. Shin, S. Cho, I. Hwang, Y. Kim, and S. Oh. 2020. “Molecular Characterization of Microbial and Fungal Communities on Dry‐Aged Beef of Hanwoo Using Metagenomic Analysis.” Foods 9: 1571. https://doi.org/10.3390/foods9111571.
Samelis, J., and J. N. Sofos. 2003. “Yeasts in Meat and Meat Products.” In Yeasts in Food, 239–265. Elsevier. https://doi.org/10.1533/9781845698485.239.
Samson, R. A., C. M. Visagie, J. Houbraken, et al. 2014. “Phylogeny, Identification and Nomenclature of the Genus Aspergillus.” Studies in Mycology 78, no. 1: 141–173. https://doi.org/10.1016/j.simyco.2014.07.004.
Savini, F., V. Indio, F. Giacometti, et al. 2024. “Microbiological Safety of Dry‐Aged Meat: A Critical Review of Data Gaps and Research Needs to Define Process Hygiene and Safety Criteria.” Italian Journal of Food Safety 13: 12438. https://doi.org/10.4081/ijfs.2024.12438.
Setyabrata, D., B. R. Cooper, T. J. P. Sobreira, J. F. Legako, S. Martini, and Y. H. B. Kim. 2021. “Elucidating Mechanisms Involved in Flavor Generation of Dry‐Aged Beef Loins Using Metabolomics Approach.” Food Research International 139: 109969. https://doi.org/10.1016/j.foodres.2020.109969.
Toldrá, F. 1998. “Proteolysis and Lipolysis in Flavour Development of Dry‐Cured Meat Products.” Meat Science 49, no. Suppl. 1: S101–S110. https://doi.org/10.1016/S0309‐1740(98)90041‐9.
Visagie, C. M., J. Houbraken, J. C. Frisvad, et al. 2014. “Identification and Nomenclature of the Genus Penicillium.” Studies in Mycology 78, no. 1: 343–371. https://doi.org/10.1016/j.simyco.2014.09.001.
Wang, H., J. Wang, Y. Wang, et al. 2023. “Characterization and Correlation of Dominant Microbiota and Flavor Development in Different Post‐Mortem Processes of Beef.” Foods 12: 3266. https://doi.org/10.3390/foods12173266.
White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. “Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics.” In PCR Protocols, 315–322. Elsevier. https://doi.org/10.1016/B978‐0‐12‐372180‐8.50042‐1.
Yoo, Y., H. Oh, and Y. Yoon. 2023. “Isolation of Debaryomyces hansenii and Selection of an Optimal Strain to Improve the Quality of Low‐Grade Beef Rump (Middle Gluteal) During Dry Aging.” Animal Bioscience 36: 1426–1434. https://doi.org/10.5713/ab.22.0475.
Grant Information: JDC2023-052485-I Ministerio de Ciencia, Innovación y Universidades; EFA144/16/DIETAPYR2;EFA216/16ALBERAPASTUR European Regional Development Fund
Contributed Indexing: Keywords: aging; aging environment; beef; culturable mycobiota; enzymatic activity
Entry Date(s): Date Created: 20261009 Date Completed: 20261009 Latest Revision: 20261009
Update Code: 20261010
DOI: 10.1111/1750-3841.71445
PMID: 42853374
Βάση Δεδομένων: MEDLINE
Περιγραφή
ISSN:1750-3841
DOI:10.1111/1750-3841.71445