Impact of seasonality and environmental conditions on yeast diversity from camel’s milk collected in Algeria

  • Soufian Ider
  • Yanath Belguesmia
  • Françoise Coucheney
  • Mabrouk Kihal
  • Djamel DriderEmail author


During this study, we characterized the seasonality’s impact and environmental conditions on the yeast diversity from raw camel’s milk collected in Algeria. The yeast counts were estimated to 3.55 × 102 CFU mL−1, with a maximum of 6.3 × 102 CFU mL−1. The yeasts were categorized phenotypically by API 20C AUX, MALDI-TOF and genetically by sequencing 26S rDNA and ITS1-5.8S-ITS2. The rDNA sequencing approaches revealed 12 species including unusual ones such as Trichosporon asahii, Pichia fermentans, Millerozyma farinosa, Pichia galeiformis, Candida tartarivorans and Pichia manshurica. The most dominant species were T. asahii (23%), P. fermentans (19%) and Rhodotorula mucilaginosa (14%). The high occurrence and large diversity were registered in samples collected during the autumn season, in the semi-arid and arid highlands regions with 0.66 × 103 CFU mL−1 and 0.51 × 103 CFU mL−1, respectively. Interestingly, T. asahii, R. mucilaginosa, P. fermentans, C. parapsilosis and C. zeylanoides were detected during both spring and autumn.


Camel milk Yeasts Biodiversity Environmental conditions Phenotypic and genotypic characterization 



Sofian Ider received a short-term PhD Grant from the Algerian Government. The authors are indebted to la region des Hauts-de-France through CPER/FEDER Alibiotech Grant [2016–2020], allowing experimental work at Lille University as well as support postdoctoral position of Dr. Yanath Belguesmia. The authors are indebted to Dr. Bruce Seal (Oregon State University Cascades) for critical reading of the manuscript.


  1. Abdelgadir W, Nielsen DS, Hamad S, Jakobsen M (2008) A traditional sudanese fermented camel’s milk product, gariss, as a habitat of Streptococcus Infantarius subsp. Infantarius. Int J Food Microbiol 127:215–219CrossRefGoogle Scholar
  2. Akdouche L, Aissi M, Zenia S, Saadi A (2014) Importance of yeasts in the mammary infection of the cattle in the region of Sidi M’hamed Ben Ali, Wilaya Of Relizane, Algeria. J Vet Sci Technol 5:2. Google Scholar
  3. Angulo FJ, Lejeune JT, Rajala-Schultz PJ (2009) Unpasteurized milk: a continued public health threat. Clin Infect Dis 48:93–100CrossRefGoogle Scholar
  4. Ashengroph M, Amini J (2017) Bioconversion of isoeugenol to vanillin and vanillic acid using the resting cells of Trichosporon asahii. Biotech 7:358Google Scholar
  5. Barnett JA, Payne RW, Yarrow D (1983) Yeasts: characteristics and identification. University Press, CambridgeGoogle Scholar
  6. Baroiller C, Schmidt JL (1990) Contribution à l’étude de l’origine des levures du fromage de Camembert. Lait 70:67–84CrossRefGoogle Scholar
  7. Bockelmann W, Heller M, Heller KJ (2008) Identification of yeasts of dairy origin by amplified ribosomal DNA restriction analysis (Ardra). Int Dairy J 18:1066–1071CrossRefGoogle Scholar
  8. Callon C, Duthoit F, Delbès C, Ferrand M, Le Frileux Y, De Crémoux R, Montel MC (2007) Stability of microbial communities in goat milk during a lactation year: molecular approaches. Syst Appl Microbiol 30:547–560CrossRefGoogle Scholar
  9. Cardoso VM, Borelli BM, Lara CA, Soares MA, Pataro C, Bodevan EC, Rosa CA (2015) The influence of seasons and ripening time on yeast communities of a traditional Brazilian Cheese. Food Res Int 69:331–340CrossRefGoogle Scholar
  10. Ceugniez A, Drider D, Jacques P, Coucheney F (2015) Yeast diversity in a traditional French Cheese “Tomme D’orchies” reveals infrequent and frequent species with associated benefits. Food Microbiol 52:177–184CrossRefGoogle Scholar
  11. Chen LS, Ma Y, Maubois JL, He SH, Chen LJ, Li HM (2010a) Screening for the potential probiotic yeast strains from raw milk to assimilate cholesterol. Dairy Sci Tech 90:537–548CrossRefGoogle Scholar
  12. Chen LS, Ma Y, Maubois JL, Chen LJ, Liu QH, Guo JP (2010b) Identifcation Of yeasts from raw milk and selection for some specific antioxidant properties. Int J Dairy Tech 63:47–54CrossRefGoogle Scholar
  13. Chen LS, Cui J, Ding QB, Ma Y, Chen LJ, Dong JY, Jiang TM, Maubois JL (2012) The effect of yeast species from raw milk in china on proteolysis and aroma compound formation in Camembert-type cheese. Food Bioproc Tech 5:2548–2556CrossRefGoogle Scholar
  14. Coorevits A, De Jonghe V, Vandroemme J, Reekmans R, Heyrman J, Messens W, De Vos P, Heyndrickx M (2008) comparative analysis of the diversity of aerobic spore-forming bacteria in raw milk from organic and conventional dairy farms. Syst Appl Microbiol 31:126–140CrossRefGoogle Scholar
  15. Cosentino S, Fadda ME, Deplano M, Mulargia A, Palmas F (2001) Yeasts Associated with Sardinian Ewe’s dairy products. Int J Food Microbiol 69:53–58CrossRefGoogle Scholar
  16. De Freitas I, Pinon N, Berdagué JL, Tournayre P, Lortal S, Thierry A (2008) Kluyveromyces lactis but not Pichia fermentans used as adjunct culture modifies the olfactory profiles of cantalet cheese. J Dairy Sci 91:531–543CrossRefGoogle Scholar
  17. De Freitas I, Pinon N, Maubois JL, Lortal S, Thierry A (2009) The addition of a cocktail of yeast species to cantalet cheese changes bacterial survival and enhances aroma compound formation. Int J Food Microbiol 129:37–42CrossRefGoogle Scholar
  18. Delavenne E, Mounier J, Asmani K, Jany JL, Barbier G, Le Blay G (2011) Fungal diversity in cow, goat and ewe milk. Int J Food Microbiol 151:247–251CrossRefGoogle Scholar
  19. Elhassan B, Ayat M, Dahan T, Smahi K (2013) Level of control of the hygienic quality of camel milk (Camelus dromedarius) in South West Algeria And its impact on security. Peak J Food Sci Tech 1:53–60Google Scholar
  20. El-Jakee J (1998) Microbiological Studies on mammary glands of one humped she-camels in Egypt. J Camel Pract Res 5:243–246Google Scholar
  21. Fadda ME, Viale S, Deplano M, Pisano MB, Cosentino S (2010) Characterization of yeast population and molecular fingerprinting of Candida zeylanoides isolated from goat’s milk collected in Sardinia. Int J Food Microbiol 136:376–380CrossRefGoogle Scholar
  22. Haddadin MS, Gammoh SI, Robinson RK (2008) Seasonal variations in the chemical composition of camel milk in Jordan. J Dairy Res 75:8–12CrossRefGoogle Scholar
  23. Harju S, Fedosyuk H, Peterson KR (2004) Rapid isolation of yeast genomic DNA: bust N’grab. BMC Biotechnol 4:8CrossRefGoogle Scholar
  24. Jespersen L, Nielsen DS, Hønholt S, Jakobsen M (2005) Occurrence and diversity of yeasts involved in fermentation of West African Cocoa Beans. FEMS Yeast Res 5:441–453CrossRefGoogle Scholar
  25. Konuspayeva G, Faye B, Loiseau G (2009) The composition of camel milk: a meta-analysis of the literature data. J Food Composition Anal 22:95–101CrossRefGoogle Scholar
  26. Ksouri S, Djebir S, Hadef Y, Benakhla A (2015) Survey of bovine mycotic mastitis in different mammary gland statuses in two North-Eastern Regions of Algeria. Mycopathologia 179:327–331CrossRefGoogle Scholar
  27. Kurtzman C, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study. Elsevier, NYGoogle Scholar
  28. Lagneau P, Lebtahi K, Swinne D (1996) Isolation of yeasts from bovine milk in Belgium. Mycopathologia 135:99–102CrossRefGoogle Scholar
  29. Lavoie K, Touchette M, St-Gelais D, Labrie S (2012) Characterization of the fungal microflora in raw milk and specialty cheeses of the province of Quebec. Dairy Sci Tech 92:455–468CrossRefGoogle Scholar
  30. Lhoste F (2004) Lait De Chamelle Pour L’afrique. Fao Brochure Google Scholar
  31. Lopandic K, Zelger S, Bánszky LK, Eliskases-Lechner F, Prillinger H (2006) Identification of yeasts associated with milk products using traditional and molecular techniques. Food Microbiol 23:341–350CrossRefGoogle Scholar
  32. Lore TA, Mbugua SK, Wangoh J (2005) Enumeration and identification of microflora in Suusac, a Kenyan traditional fermented camel milk product. Lwt-Food Sci Tech 38:125–130CrossRefGoogle Scholar
  33. Motulsky H (1999) Analyzing data with graphpad prism, Graphpad Software IncorporatedGoogle Scholar
  34. Mu Z, Yang X, Yuan H (2012) Detection and identification of wild yeast in koumiss. Food Microbiol 31:301–308CrossRefGoogle Scholar
  35. Njage P, Dolci S, Jans C, Wangoh J, Lacroix C, Meile L (2011) Characterization of yeasts associated with camel milk using phenotypic and molecular identification techniques. Res J Microbiol 6:678CrossRefGoogle Scholar
  36. O’Sullivan O, Cotter PD (2017) Microbiota of raw milk and raw milk cheeses. In: Cheese (Fourth Edition). Elsevier, NYGoogle Scholar
  37. Pal M (2015) First record of camel mastitis due to Candida albicans in Ethiopia. Indian J Comp Microbiol Immunol Infect Dis 3632–34Google Scholar
  38. Park YW, Haenlein GF (2008) Handbook of milk of non-bovine mammals. Blackwell Publishing, Wiley, Ames, IowaGoogle Scholar
  39. Qvirist LA, De Filippo C, Strati F, Stefanini I, Sordo M, Andlid T, Felis GE, Mattarelli P, Cavalieri D (2016) Isolation, identification and characterization of yeasts from fermented goat milk of the Yaghnob Valley in Tajikistan. Front Microbiol 7:1690CrossRefGoogle Scholar
  40. Rahman N, Xiaohong C, Meiqin F, Mingsheng D (2009) Characterization of the dominant microflora in naturally fermented camel milk shubat. World J Microbiol Biotechnol 25:1941–1946CrossRefGoogle Scholar
  41. Rodrigues C, Yarrow D, Spencer-Martins I (1996) Nuclear DNA comparisons among strains of Pichia membranifaciens. In: Abstr. 9th International symposium on yeasts, 1996. 31Google Scholar
  42. Roostita R, Fleet G (1996) The occurrence and growth of yeasts in camembert and blue-veined cheeses. Int J Food Microbiol 28:393–404CrossRefGoogle Scholar
  43. Schwan RF, Almeida EG, Souza-Dias MAG, Jespersen L (2007) Yeast diversity In Rice–Cassava fermentations produced by the Indigenous Tapirapé people of Brazil. FEMS Yeast Res 7:966–972CrossRefGoogle Scholar
  44. Siboukeur O (2007) Etude Du Lait Camelin Collecté Localement: Caractéristiques Physico-Chimiques Et Microbiologiques; Aptitudes A La Coagulation. Thèse De Doctorat, Institut National Agronomique, El-Harrach-Algeria, p 22Google Scholar
  45. Singh Y, Gupta R (2016) Novel S-enantioselective lipase TALipB from Trichosporon asahii MSR54: heterologous expression, characterization, conformational stability and homology modeling. Enzyme Microb Technol 83:29–39CrossRefGoogle Scholar
  46. Suzzi G, Schirone M, Martuscelli M, Gatti M, Fornasari ME, Neviani E (2003) Yeasts associated with Manteca. FEMS Yeast Res 3:159–166CrossRefGoogle Scholar
  47. Tourette I, Messad S, Faye B (2002) Impact Des Pratiques De Traite Des Eleveurs Pur La Qualité Sanitaire Du Lait De Chamelle En Mauritanie. Revue Élev Méd Vét Pays Trop 55:229–233Google Scholar
  48. Vacheyrou M, Normand AC, Guyot P, Cassagne C, Piarroux R, Bouton Y (2011) Cultivable microbial communities in raw cow milk and potential transfers from stables of sixteen French farms. Int J Food Microbiol 146:253–262CrossRefGoogle Scholar
  49. Valle RS, Ramos LS, Reis VJ, Ziccardi M, Dornelas-Ribeiro M, Sodré CL, Branquinha MH, Santos ALS (2017) Trichosporon asahii secretes a 30-kDa aspartic peptidase. Microbiol Res 205:66–72CrossRefGoogle Scholar
  50. Vasdinyei R, Deak T (2003) Characterization of yeast isolates originating from Hungarian dairy products using traditional and molecular identification techniques. Int J Food Microbiol 86:123–130CrossRefGoogle Scholar
  51. Watanabe K, Fujimoto J, Sasamoto M, Dugersuren J, Tumursuh T, Demberel S (2008) Diversity of lactic acid bacteria and yeasts in airag and tarag, traditional fermented milk products of Mongolia. World J Microbiol Biotechnol 24:1313–1325CrossRefGoogle Scholar
  52. Yam BZ, Khomeiri M, Mahounak AS, Jafari SM (2015) Isolation and identification of yeasts and lactic acid bacteria from local traditional fermented camel milk, Chal. J Food Process Technol 6:460.
  53. Zaragoza CS, Olivares RAC, Watty AED, De La Peña Moctezuma A, Tanaca LV (2011) Yeasts isolation from bovine mammary glands under different mastitis status in the Mexican high plateu. Rev Iberoam Micol 28:79–82CrossRefGoogle Scholar
  54. Zhang Y, Li H, Yang R, Wang C (2016) Study on Antioxidant Enzymatic Activities of Trichosporon asahii. Indian J Microbiol 56:445–450CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Soufian Ider
    • 1
    • 2
    • 3
  • Yanath Belguesmia
    • 2
  • Françoise Coucheney
    • 2
  • Mabrouk Kihal
    • 1
  • Djamel Drider
    • 2
    Email author
  1. 1.Laboratoire de Microbiologie Fondamentale et Appliquée, Faculté des Sciences de la Nature et de la VieUniversité Oran 1 - Ahmed Ben BellaOranAlgeria
  2. 2.EA 7394-Institut Charles VioletteUniversité de LilleLilleFrance
  3. 3.Département de Biologie, Faculté des Sciences de la Nature et de la Vie et Sciences de la TerreUniversité de GhardaïaGhardaïaAlgeria

Personalised recommendations