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Raw goat's milk fermented Anbaris from Lebanon: insights into the microbial dynamics and chemical changes occurring during artisanal production, with a focus on yeasts

Published online by Cambridge University Press:  23 November 2022

Marie-José Ayoub ,
Pamela Bechara ,
Mariana Habchi ,
Rachelle Hosry ,
Mohamad Akl ,
Sandy Haj Hassan  and
Pierre Abi Nakhoul
Marie-José Ayoub
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
Pamela Bechara
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
Mariana Habchi
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
Rachelle Hosry
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
Mohamad Akl
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
Sandy Haj Hassan
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
Pierre Abi Nakhoul*
Affiliation:
Department of Food Sciences and Technologies, Faculty of Agricultural and Veterinary Sciences, Lebanese University, 7 14/6573, Beirut, Lebanon
*
Author for correspondence: Pierre Abi Nakhoul, Email: pabinakhoul@ul.edu.lb
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Abstract

Anbaris is a raw goat milk product naturally fermented in terracotta jars. The aim of this research paper was to follow the dynamics underlying an artisanal production to understand the concomitant evolution of the microbial populations in relation to the chemical changes occurring within the product, make sure of the sanitary conditions prevailing during the production and uncover for the first time its culturable yeast populations. Throughout the fermentation process, Anbaris was endowed with high acidity and included high microbial populations counts of LAB and yeasts that were rapidly installed within the product and maintained as regular new milk additions were made, contributing to lipolytic and proteolytic activities. Salt content varied according to the arbitrary salt additions made during the process but was high in the end product while protein and fat contents varied inversely to moisture. Frequent additions of Enterobacteriaceae and Coliforms contaminated milk samples seemingly fueled a contamination of the product during its manufacturing and in the final fresh Anbaris. Seven species of culturable yeasts, Pichia kudriavzevii, Kluyveromyces marxianus, Rhodotorula mucilaginosa, Saccharomyces cerevisiae, Debaryomyces hansenii, Candida parapsilosis and Kazachstania exigua were found during the production. The first two dominated the process in terms of frequency of occurrence and abundance at the different stages and might be signature species of the product. The same lineage of K. marxianus isolates was maintained throughout the fermentation and sample specific patterns were observed. Strains of this species exhibited low diversity within our product, and more globally in the Lebanese dairy products we studied.

Keywords

Chemical changesfermented goat milkKluyveromyces marxianusmicrobial dynamicsraw milk cheeseyeast diversity
Type
Research Article
Information
Journal of Dairy Research , Volume 89 , Issue 4 , November 2022 , pp. 440 - 448
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Hannah Dairy Research Foundation

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References

Abiad, M, Ajjour, C, Kassaify, Z, Iskandar, C, Hamzeh, R and Hassan, H (2022) Preliminary physiological, phenotypic, and probiotic characterization of Lactobacillus strains isolated from Anbaris-traditional Lebanese fermented dairy product. International Journal of Food Properties 25, 1266–1278.CrossRefGoogle Scholar
Akuzawa, R, Miura, T and Surono, IS (2022) Asian fermented milk. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 404–408.CrossRefGoogle Scholar
Álvarez-Martín, P, Flórez, A, Hernández-Barranco, A and Mayo, B (2008) Interaction between dairy yeasts and lactic acid bacteria strains during milk fermentation. Food Control 19, 62–70.CrossRefGoogle Scholar
Arias-Roth, E, Bachmann, HP, Fröhlich-Wyder, MT, Schmidt, RS, Wechsler, D, Beuvier, E, Buchin, S and Delbès, C (2022) Cheese: raw milk cheeses. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 299–308.CrossRefGoogle Scholar
Ayoub, M-J, Legras, J-L, Abi Nakhoul, P, Nguyen, HV, Saliba, R and Gaillardin, C (2021) Lebanon's native oenological Saccharomyces cerevisiae flora: assessment of different aspects of genetic diversity and evaluation of winemaking potential. Journal of Fungi 7, 678.CrossRefGoogle ScholarPubMed
Bai, M, Qing, M, Guo, Z, Zhang, Y, Chen, X, Bao, Q, Zhang, H and Sun, TS (2010) Occurrence and dominance of yeast Species in naturally fermented milk from the Tibetan plateau of China. Canadian Journal of Microbiology 56, 707–714.CrossRefGoogle ScholarPubMed
Betts, G, Everis, L and Betts, R (2007) Microbial issues in reducing salt in food products. In Kilcast, D and Angus, F (eds), Woodhead Publishing Series in Food Science, Technology and Nutrition, Reducing Salt in Foods. UK: Woodhead Publishing CCFRA, pp. 174–200.Google Scholar
Bintsis, T (2021) Yeasts in different types of cheese. AIMS Microbiology 7, 447–470.CrossRefGoogle ScholarPubMed
Bokulich, NA and Mills, DA (2013) Facility-specific ‘house’ microbiome drives microbial landscapes of artisan cheesemaking plants. Applied Environmental Microbiology 79, 5214–5223.Google ScholarPubMed
Broadbent, JR (2022) Non-starter lactic acid bacteria. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 245–249.CrossRefGoogle Scholar
Büchl, NR and Seiler, H (2011) Yeasts and molds: yeasts in milk and dairy products. In Fuquay, JW (ed.), Encyclopedia of Dairy Sciences, 2nd Edn. London: Elsevier Ltd, Academic Press, pp. 744–753.Google Scholar
Bütikofer, U, Rüegg, M and Ardö, Y (1993) Determination of nitrogen fractions in cheese: evaluation of a collaborative study. LWT – Food Science and Technology 26, 271–275.CrossRefGoogle Scholar
Buzzini, P, Turchetti, B and Yurkov, A (2018) Extremophilic yeasts: the toughest yeasts around? Yeast 35, 487–497.CrossRefGoogle ScholarPubMed
Cakebread, JA (2022) Health effects of fermented milks. In Encyclopedia of Dairy Sciences, 3rd Edn. McSweeney, PLH and McNamara, JP (eds), London: Elsevier Ltd, Academic Press, 430–437.CrossRefGoogle Scholar
Cardoso, VM, Borelli, BM, Lara, CA, Soares, MA, Pataro, C, Bodevan, EC and Rosa, CA (2015) The influence of seasons and ripening time on yeast communities of a traditional Brazilian cheese. Food Research International 69, 331–340.CrossRefGoogle Scholar
Colonna, A, Durham, C and Meunier-Goddik, L (2011) Factors affecting consumers’ preferences for and purchasing decisions regarding pasteurized and raw milk specialty cheeses. Journal of Dairy Science 94, 5217–5226.Google ScholarPubMed
Coolbear, T, Wilkinson, MG and Weimer, B (2022) Lactic acid bacteria in flavor development. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 181–186.CrossRefGoogle Scholar
Costanzo, N, Ceniti, C, Santoro, A, Clausi, MT and Casalinuovo, F (2020) Foodborne pathogen assessment in raw milk cheeses. International Journal of Food Science 2020, 3616713.CrossRefGoogle ScholarPubMed
Criste, A, Copolovici, L, Copolovici, D, Kovacs, M, Madden, RH, Corcionivoschi, N, Gundogdu, O, Berchez, M and Urcan, AC (2020) Determination of changes in the microbial and chemical composition of Țaga cheese during maturation. PLoS ONE 15(12), e0242824.CrossRefGoogle ScholarPubMed
De Freitas, I, Pinon, N, Maubois, JL, Lortal, S and Thierry, A (2009) The addition of a cocktail of yeast species to Cantalet cheese changes bacterial survival and enhances aroma compound formation. International Journal of Food Microbiology 129, 37–42.CrossRefGoogle ScholarPubMed
Dimassi, O, Iskandarani, Y, Afram, M, Akiki, R and Rached, M (2020a) Production and physicochemical properties of Labneh Anbaris, a traditional fermented cheese like product, in Lebanon. International Journal of Environment, Agriculture and Biotechnology 5, 509–516.CrossRefGoogle Scholar
Dimassi, O, Iskandarani, Y and Akiki, RP (2020b) Effect of followed production procedures on the physicochemical properties of Labneh Anbaris. International Journal of Environment Agriculture and Biotechnology 5, 1430–1437.CrossRefGoogle Scholar
El-Sharoud, WM, Belloch, C, Peris, D and Querol, A (2009) Molecular identification of yeasts associated with traditional Egyptian dairy products. Journal of Food Science 74, M341–M346.CrossRefGoogle ScholarPubMed
Esteve-Zarzoso, B, Belloch, C, Uruburu, F and Querol, A (1999) Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. International Journal of Systematic Bacteriology 49(Pt 1), 329–337.Google ScholarPubMed
Fernández, M, Hudson, JA, Korpela, R and de los Reyes-Gavilán, CG (2015) Impact on human health of microorganisms present in fermented dairy products: an overview. BioMed Research International 2015, 412714.CrossRefGoogle ScholarPubMed
Fröhlich-Wyder, MT, Arias-Roth, E and Jakob, E (2019) Cheese yeasts. Yeast 36, 129–141.CrossRefGoogle ScholarPubMed
García-Cano, I, Rocha-Mendoza, D, Ortega-Anaya, J, Wang, K, Kosmerl, E and Jiménez-Flores, R (2019) Lactic acid bacteria isolated from dairy products as potential producers of lipolytic, proteolytic and antibacterial proteins. Applied Microbiology and Biotechnology 103, 5243–5257.CrossRefGoogle ScholarPubMed
Guinee, TP and Sutherland, BJ (2022) Salting of cheese. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd., Academic Press, pp. 321–335.CrossRefGoogle Scholar
Hayaloglu, AA, Guven, M, Fox, PF and McSweeney, PL (2005) Influence of starters on chemical, biochemical, and sensory changes in Turkish White-brined cheese during ripening. Journal of Dairy Science 88, 3460–3474, Erratum in: Journal of Dairy Science 2006; 89 2353.CrossRefGoogle ScholarPubMed
Heaney, H, Laing, J, Paterson, L, Walker, A, Gow, N, Johnson, E, MacCallum, D and Brown, A (2020) The environmental stress sensitivities of pathogenic Candida species, including Candida auris, and implications for their spread in the hospital setting. Medical Mycology 58, 744–755.CrossRefGoogle ScholarPubMed
Hoffman, CS (2001) Preparation of yeast DNA. Current Protocols in Molecular Biology, section IV, Unit13.11, 1–4.Google ScholarPubMed
Juillard, V, Lopez-Kleine, L and Monnet, M (2022) Lactic acid bacteria: proteolytic systems. In Encyclopedia of Dairy Sciences, 3rd Edn. McSweeney, PLH and McNamara, JP (eds), London: Elsevier Ltd, Academic Press, pp. 249–255.CrossRefGoogle Scholar
Lavoie, K, Touchette, M, St-Gelais, D and Labrie, S (2012) Characterization of the fungal microflora in raw milk and specialty cheeses of the Province of Quebec. Dairy Science & Technology 92, 455–468.CrossRefGoogle ScholarPubMed
Li, J, Huang, Q, Zheng, X, Ge, Z, Lin, K, Zhang, D, Chen, Y, Wang, B and Shi, X (2020) Investigation of the lactic acid bacteria in Kazak cheese and their contributions to cheese fermentation. Frontiers in Microbiology 11, 228.CrossRefGoogle ScholarPubMed
Licitra, G (2010) Worldwide traditional cheeses: banned for business? Dairy Science & Technology, EDP Sciences/Springer 90, 357–374.CrossRefGoogle Scholar
Lucey, JA (2022) Acid- and acid/heat coagulated cheese. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 6–14.CrossRefGoogle Scholar
McSweeney, PLH (2022) Biochemistry of cheese ripening. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 22–29.CrossRefGoogle Scholar
Merchán, A, Ruiz-Moyano, S, Hernández, MV, Benito, MJ, Aranda, E, Rodríguez, A and Martín, A (2022) Characterization of autochthonal yeasts isolated from Spanish soft raw ewe milk protected designation of origin cheeses for technological application. Journal of Dairy Science 4, 2931–2947, 111.CrossRefGoogle Scholar
Metz, M, Sheehan, J and Feng, P (2020) Use of indicator bacteria for monitoring sanitary quality of raw milk cheeses – a literature review. Food Microbiology 85, 103283.CrossRefGoogle ScholarPubMed
Mladenović, KG, Grujović, M, Kiš, M, Furmeg, S, Jaki Tkalec, V, Stefanović, OD and Kocić-Tanackov, SD (20220 Enterobacteriaceae in food safety with an emphasis on raw milk and meat. Applied Microbiology and Biotechnology 105, 8615–8627.CrossRefGoogle Scholar
Montel, MC, Buchin, S, Mallet, A, Delbès-Paus, C, Vuitton, DA, Desmasures, N and Berthier, F (2014) Traditional cheeses: rich and diverse microbiota with associated benefits. International Journal of Food Microbiology 177, 136–154.CrossRefGoogle ScholarPubMed
Mounier, J and Coton, M (2022) Kluyveromyces spp. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 569–574.CrossRefGoogle Scholar
Navarrete, C and Martínez, JL (2020) Non-conventional yeasts as superior production platforms for sustainable fermentation based bio-manufacturing processes. AIMS Bioengineering 7, 289–305.CrossRefGoogle Scholar
Nazzaro, F, Fratianni, F, Cozzolino, R, Martignetti, A, Malorni, L, De Feo, V, Cruz, AG and d'Acierno, A (2019) Antibacterial activity of three extra virgin olive oils of the campania region, southern Italy, related to their polyphenol content and composition. Microorganisms 7, 321.CrossRefGoogle ScholarPubMed
Nyambane, B, Thari, WM, Wangoh, J and Njage, PM (2014) Lactic acid Bacteria and yeasts involved in the fermentation of Amabere Amaruranu, a Kenyan fermented milk. Food Science & Nutrition 2, 692–699.CrossRefGoogle ScholarPubMed
Olajide, A and LaPointe, G (2022) Microorganisms associated with raw milk. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 319–328.CrossRefGoogle Scholar
Péter, G and Rosa, C (Eds) (2006) Environmental Factors Influencing Yeasts. Biodiversity and Ecophysiology of Yeasts. s.l. : Springer, Berlin, Heidelberg, 2006.Google Scholar
Quigley, L, O'Sullivan, O, Stanton, C, Beresford, TP, Ross, RP, Fitzgerald, GF and Cotter, PD (2013) The complex microbiota of raw milk. FEMS Microbiology Reviews 37, 664–698.CrossRefGoogle ScholarPubMed
Radecka, D, Mukherjee, V, Mateo, R, Stojiljkovic, M, Foulquié-Moreno, M and Thevelein, M (2015) Looking beyond Saccharomyces: the potential of non-conventional yeast species for desirable traits in bioethanol fermentation. FEMS Yeast Research 15(6) https://doi.org/10.1093/femsyr/fov053.CrossRefGoogle ScholarPubMed
Rako, A, Kalit, MT, Rako, Z, Zamberlin, S and Kalit, S (2022) Contribution of salt content to the ripening process of Croatian hard sheep milk cheese (Brač cheese) LWT – Food Science and Technology 162, 113506.Google Scholar
Rattray, FP and O'Connell, MJ (2022) Kefir. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of dairy sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 438–445.CrossRefGoogle Scholar
Richardson, GH (1985) Standard Methods for the Examination of Dairy Products. 15th Edition, Committee on Laboratory Standards and Practices, American Public Health Association, Washington DC, p. 327.Google Scholar
Ritschard, JS, Van Loon, H, Amato, L, Meile, L and Schuppler, M (2022) High prevalence of Enterobacterales in the smear of surface-ripened cheese with contribution to organoleptic properties. Foods (Basel, Switzerland) 11, 361.Google ScholarPubMed
Roos, YH (2022) Water in dairy products: significance. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 629–636.CrossRefGoogle Scholar
Russo, G, Libkind, D, Sampaio, JP and van Broock, MR (2008) Yeast diversity in the acidic Rio Agrio–Lake Caviahue volcanic environment (Patagonia, Argentina). FEMS Microbiology Ecology 65, 415–424.CrossRefGoogle ScholarPubMed
Serhan, M and Mattar, J (2013) Characterization of four Lebanese artisanal goat milk cheeses: Darfiyeh, Aricheh, Shankleesh and Serdale by physico-chemical, microbiological and sensory analyses. Journal of Food Agriculture and Environment 11, 97–101.Google Scholar
Serhan, M, Cailliez-Grimal, C, Borges, F, Revol-Junelles, A-M, Hosri, C and Fanni, J (2009) Bacterial diversity of Darfiyeh, a Lebanese artisanal raw goat's milk cheese. Food Microbiology 26, 645–652.Google ScholarPubMed
Sessou, P (2022) Yeasts in milk and dairy products. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 611–617.CrossRefGoogle Scholar
Siedler, S, Rau, MH, Bidstrup, S, Vento, JM, Aunsbjerg, SD, Bosma, EF, McNair, LM, Beisel, CL and Neves, AR (2020) Competitive exclusion is a major bioprotective mechanism of Lactobacilli against fungal spoilage in fermented milk products. Applied and Environmental Microbiology 86(7), e02312–19.Google Scholar
Sohier, D, Le Dizes, A-S, Thuault, D, Neuveglise, C, Coton, E and Casaregola, S (2009) Important genetic diversity revealed by inter-LTR PCR fingerprinting of Kluyveromyces marxianus and Debaryomyces hansenii strains from French traditional cheeses. Dairy Science and Technology 89, 569–581.Google Scholar
Soltani, M, Guzeler, N and Hayaloglu, AA (2015) The influence of salt concentration on the chemical, ripening and sensory characteristics of Iranian white cheese manufactured by UF-treated milk. Journal of Dairy Research 82, 365–374.CrossRefGoogle ScholarPubMed
Stratford, M, Steels, H, Novodvorska, M, Archer, DB and Avery, SV (2019) Extreme osmotolerance and halotolerance in food-relevant yeasts and the role of glycerol-dependent cell individuality. Frontiers in Microbiology 9, 3238.CrossRefGoogle ScholarPubMed
Tabet, E, Salameh, C, Nehme, M, Daher, J and Hosri, C (2019) Innovation Aspects of Serdaleh, a Traditional Lebanese Cheese Produced from Raw Extensive Goat's Milk. Options Méditerranéennes, A, no. 123 Innovations for Sustainability in Sheep and Goats, 299–304.Google Scholar
Tang, H, Ma, H, Hou, Q, Li, W, Xu, H, Liu, W, Sun, Z, Haobisi, H and Menghe, B (2020) Profiling of Koumiss microbiota and organic acids and their effects on Koumiss taste. BMC Microbiology 20, 85.CrossRefGoogle ScholarPubMed
Tittarelli, F, Varela, JA, Gethins, L, Stanton, C, Ross, RP, Suzzi, G, Grazia, L, Tofalo, R and Morrissey, JP (2018) Development and implementation of multilocus sequence typing to study the diversity of the yeast Kluyveromyces marxianus in Italian cheeses. Microbial genomics 4(2), e000153.CrossRefGoogle Scholar
Togay, OS, Capece, A, Siesto, G, Sandikci, AH, Yilmaz, AF, Romano, P and Karagul, YY (2020) Molecular characterization of yeasts isolated from traditional Turkish cheeses. Food Science and Technology 40, 871–876.CrossRefGoogle Scholar
Uniacke-Lowe, T (2022) Koumiss. In McSweeney, PLH and McNamara, JP (eds), Encyclopedia of Dairy Sciences, 3rd Edn. London: Elsevier Ltd, Academic Press, pp. 446–452.CrossRefGoogle Scholar
Viljoen, BC (2001) The interaction between yeasts and bacteria in dairy environments. International Journal of Food Microbiology 69, 37–44.CrossRefGoogle ScholarPubMed
Wouters, JT, Ayad, EH, Hugenholtz, J and Smit, G (2002) Microbes from raw milk for fermented dairy products. International Dairy Journal 12, 91–109.CrossRefGoogle Scholar
Xiao, J, Chen, Y, Li, J, Shi, X, Deng, L and Wang, B (2020) Evaluation of the effect of auxiliary starter yeasts with enzyme activities on Kazak cheese quality and flavor. Frontiers in Microbiology 11, 614208.CrossRefGoogle ScholarPubMed
Yoon, Y, Lee, S and Choi, KH (2016) Microbial benefits and risks of raw milk cheese. Food Control 63, 201–215.CrossRefGoogle Scholar
Zheng, X, Li, K, Shi, X, Ni, Y, Li, B and Zhuge, B (2018) Potential characterization of yeasts isolated from Kazak artisanal cheese to produce flavoring compounds. Microbiology Open 7(1), e00533.CrossRefGoogle ScholarPubMed
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