POTENTIAL TECHNOLOGICAL INTEREST OF INDIGENOUS LACTIC ACID BACTERIA FROM ALGERIAN CAMEL MILK
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Keywords
Abstract
Nine isolates of lactic acid bacteria (LAB) obtained from the predominant microbiota of different camel milk samples collected in south west Algeria, were selected in accordance with their growth ability in (cow) milk. The isolates were phenotypically and genotypically assigned to the following species: 4 Leuconostoc mesenteroides subsp. dextranicum; 2 Lactobacillus brevis; 2 Lb. plantarum; and 1 Lactococcus lactis subsp. lactis. One isolate from each of the Leuconostoc and Lactobacillus species were selected on the basis of their highest proteolytic and aminopeptidase activities. The selected isolates were used in combination with a commercial mesophilic O-type culture to make fermented milks. Sulfury flavor was detected as predominant in the sensory analysis of the milks made with only the Ln. mesenteroides and Lb. brevis adjuncts, which were characterized by the highest relative abundances of sulfur volatile compounds. Butter flavor was perceived in the milks made with the Lb. plantarum(cit+) adjunct, and was related to the presence of acetoin. Finally, cheese flavor prevailed in the milks made with both the Lb. brevis and the Lb. plantarum adjuncts, characterized by their high contents of short-chain free fatty acids. The results suggest the potential interest of these microorganisms in the manufacture of dairy products, particularly the combination of the Lb. brevis and Lb. plantarum isolates for cheese making.
Riferimenti bibliografici
Akhmetsadykova S.H., Baubekova A., Konuspayeva G., Akhmetsadykova N., Faye B. and Loiseau G. 2015. Lactic acid bacteria biodiversity in raw and fermented camel milk. Afr. J. Food Sci. Technol. 6(3): 84. http://dx.doi.org/10.14303/ajfst.2015.026.
Arahal D.R., Sánchez E., Macián M.C. and Garay E. 2008. Value of recN sequences for species identification and as a phylogenetic marker within the family “Leuconostocaceae”. Int. Microbiol. 11(1): 33. http://dx.doi.org/10.2436/20.1501.01.42.
Ashmaig A., Hasan A. and El Gaali E. 2009. Identification of lactic acid bacteria isolated from traditional Sudanese fermented camel’s milk (Gariss). Afr. J. Microbiol. Res. 3(8): 451.
Bendimerad N., Kihal M. and Berthier F. 2012. Isolation, identification, and technological characterization of wild leuconostocs and lactococci for traditional Raib type milk fermentation. Dairy Sci. Technol. 92(3): 249. http://dx.doi.org/10.1007/s13594-012-0063-8.
Boudjenah-Haroun S., Laleye C.L., Senoussi C., Moulti Mati F., Si Ahmed S. and Mati A. 2012. Coagulation of camel milk using dromedary gastric enzymes as a substitute of the commercial rennet. Am. J. Food Technol. 7(7): 409. http://dx.doi.org/10.3923/ajft.2012.409.419.
Buffa M., Guamis B., Saldo J. and Trujillo A.J. 2004. Changes in organic acids during ripening of cheeses made from raw, pasteurized or high-pressure-treated goats’ milk. Lebensm. Wiss. Technol. 37(2): 247. http://dx.doi.org/10.1016/j.lwt.2003.08.006.
Centeno J.A., Gaya P., Medina M. and Núñez M. 2002. Cross-inhibition among wild strains of Lactococcus lactis isolated from the same ecological niche. J. Food Protect. 65(1): 205.
Church F.C., Swaisgood H.E., Porter D.H. and Catignani G.L. 1983. Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J. Dairy Sci. 66(6): 1219. http://dx.doi.org/10.3168/jds.S0022-0302(83)81926-2.
Delgado F., González-Crespo J., Cava R. and Ramírez R. 2011. Formation of the aroma of a raw goat milk cheese during maturation analysed by SPME–GC–MS. Food Chem. 129(3): 1156. http://dx.doi.org/10.1016/j.foodchem.2011.05.096.
Drici H., Gilbert C., Kihal M. and Atlan D. 2010. Atypical citrate-fermenting Lactococcus lactis strains isolated from dromedary’s milk. J. Appl. Microbiol. 108(2): 647. http://dx.doi.org/10.1111/j.1365-2672.2009.04459.x.
Dutcosky S.D. 1996. “Sensory analysis of foods”. Ed. da Champagnat, Curitiba, Brasil.
El Soda M. and Desmazeaud M.J. 1982. Les peptides-hydrolases de lactobacilles du groupe Thermobacterium. 1. Mise en evidence de ces activites chez Lactobacillus helveticus, L. acidophilus, L. lactis et L. bulgaricus. Can. J. Microbiol. 28(10): 1181. http://dx.doi.org/10.1139/m82-174.
El Zubeir I.E.M. and Jabreel S.O. 2008. Fresh cheese from camel milk coagulated with Camifloc. Int. J. Dairy Technol. 61(1): 90. http://dx.doi.org/10.1111/j.1471-0307.2008.00360.x.
Engels W.J.M., Dekker R., De Jong C., Neeter R. and Visser S. 1997. A comparative study of volatile compounds in the water-soluble fraction of various types of ripened cheese. Int. Dairy J. 7(4): 255. http://dx.doi.org/10.1016/S0958-6946(97)00003-4.
FAO, 2008. Agro-statistics Database. Food and Agriculture Organization of the United Nations, Rome.
Farah Z. 1993. Composition and characteristics of camel milk. J. Dairy Res. 60(4): 603.
Farah Z. and Bachman M.R. 1987. Rennet coagulation properties of camel milk. Milchwissenschaft 42(11): 689.
Garabal J.I., Rodríguez-Alonso P. and Centeno J.A., 2008. Characterization of lactic acid bacteria isolated from raw cows’ milk cheeses currently produced in Galicia (NW Spain). LWT – Food Sci. Technol. 41(8): 1452. http://dx.doi.org/10.1016/j.lwt.2007.09.004.
González de Llano D., Rodríguez A. and Cuesta P. 1996. Effect of lactic starter cultures on the organic acid composition of milk and cheese during ripening–analysis by HPLC. J. Appl. Bacteriol. 80(5): 570. http://dx.doi.org/10.1111/j.1365-2672.1996.tb03259.x.
Herrero M., Mayo B., González B. and Suárez J.E. 1996. Evaluation of technologically important traits in lactic acid bacteria isolated from spontaneous fermentations. J. Appl. Bacteriol. 81(5): 565. http://dx.doi.org/10.1111/j.1365-2672.1996.tb03548.x.
Herreros M.A., Fresno J.M., González Prieto M.J. and Tornadijo M.E. 2003. Technological characterization of lactic acid bacteria isolated from Armada cheese (a Spanish goats’ milk cheese). Int. Dairy J. 13(6): 469. http://dx.doi.org/10.1016/S0958-6946(03)00054-2.
IDF, 1995. IDF guideline-determination of acidifying activity of dairy cultures. In: IDF Bulletin 306, p. 34-36. International Dairy Federation, Brussels.
IDF, 1997. Dairy starter cultures of lactic acid bacteria (LAB). Standard of identity. IDF Standard 149A. International Dairy Federation, Brussels.
Kaminarides S., Stamou P. and Massouras T. 2007. Changes of organic acids, volatile aroma compounds and sensory characteristics of Halloumi cheese kept in brine. Food Chem. 100(1): 219. http://dx.doi.org/10.1016/j.foodchem.2005.09.039.
Kondyli E., Massouras T., Katsiari M.C. and Voutsinas L.P. 2003. Free fatty acids and volatile compounds in low-fat Kefalograviera-type cheese made with commercial adjunct cultures. Int. Dairy J. 13(1): 47. http://dx.doi.org/10.1016/S0958-6946(02)00144-9.
Konuspayeva G., Faye B. and Loiseau G. 2009. The composition of camel milk: A meta-analysis of the literature data. J. Food Compos. Anal. 22(2): 95. http://dx.doi.org/10.1016/j.jfca.2008.09.008.
Limonet M., Cailliez-Grimal C., Linder M., Revol-Junelles A.M. and Millière J.B. 2004. Cell envelope analysis of insensitive, susceptible or resistant strains of Leuconostoc and Weissella genus to Leuconostoc mesenteroides FR 52 bacteriocins. FEMS Microbiol. Lett. 241(1): 49. http://dx.doi.org/10.1016/j.femsle.2004.10.002.
Lorenzo J.M. 2014. Influence of the type of fiber coating and extraction time on foal dry-cured loin volatile compounds extracted by solid-phase microextraction (SPME). Meat Sci. 96(1): 179. http://dx.doi.org/10.1016/j.meatsci.2013.06.017.
Lorenzo J.M. and Fonseca S. 2014. Volatile compounds of Celta dry-cured ‘lacón’ as affected by cross-breeding with Duroc and Landrace genotypes. J. Sci. Food Agr. 94(14): 2978. http://dx.doi.org/10.1002/jsfa.6643.
Macedo A.C., Vieira M., Poças R. and Malcata F.X. 2000. Peptide hydrolase system of lactic acid bacteria isolated from Serra da Estrela cheese. Int. Dairy J. 10(11): 769. http://dx.doi.org/10.1016/S0958-6946(00)00111-4.
Marco A., Navarro J.L. and Flores M. 2004. Volatile compounds of dry-fermented sausages as affected by solid-phase microextraction (SPME). Food Chem. 84(4): 633. http://dx.doi.org/10.1016/S0308-8146(03)00288-7.
McSweeney P.L.H. and Sousa M.J. 2000. Biochemical pathways for the production of flavor compounds in cheese during ripening: a review. Lait 80(3): 293. http://dx.doi.org/10.1051/lait:2000127.
Menéndez S., Centeno J.A., Godínez R. and Rodríguez-Otero J.L. 2000. Effect of Lactobacillus strains on the ripening and organoleptic characteristics of Arzúa-Ulloa cheese. Int. J. Food Microbiol. 59(1-2): 37. http://dx.doi.org/10.1016/S0168-1605(00)00286-5.
Nandan A., Gaurav A., Pandey A. and Madhavan Nampoothiri K. 2010. Arginine specific aminopeptidase from Lactobacillus brevis. Braz. Arch. Biol. Technol. 53(6): 1443. http://dx.doi.org/10.1590/S1516-89132010000600021.
Nickels C. and Leesment H. 1964. Method for the differentiation and qualitative determination of starter bacteria. Milchwissenschaft 19: 374.
Nieto-Arribas P., Seseña S., Poveda J.M., Palop L. and Cabezas L. 2009. Genotypic and technological characterization of Lactococcus lactis isolates involved in processing of artisanal Manchego cheese. J. Appl. Microbiol. 107(5): 1505. http://dx.doi.org/10.1111/j.1365-2672.2009.04334.x.
Nieto-Arribas P., Seseña S., Poveda J.M., Palop L. and Cabezas L. 2010. Genotypic and technological characterization of Leuconostoc isolates to be used as adjunct starters in Manchego cheese manufacture. Food Microbiol. 27(1): 85. http://dx.doi.org/10.1016/j.fm.2009.08.006.
Rodríguez-Alonso P., Garabal J.I. and Centeno J.A. 2008. Preliminary characterization of staphylococcal, micrococcal and yeast isolates obtained from raw cow milk cheeses currently produced in Galicia (NW Spain). Ital. J. Food Sci. 20(2): 161.
Settanni L. and Moschetti G. 2010. Non-starter lactic acid bacteria used to improve cheese quality and provide health benefits. Food Microbiol. 27(6): 691. http://dx.doi.org/10.1016/j.fm.2010.05.023.
Sreekumar R., Al-Attabi Z., Deeth H.C. and Turner M.S. 2009. Volatile sulfur compounds produced by probiotic bacteria in the presence of cysteine or methionine. Lett. Appl. Microbiol. 48(6): 777. http://dx.doi.org/10.1111/j.1472-765X.2009.02610.x.
Urbach G. 1995. Contribution of lactic acid bacteria to flavour compound formation in dairy products. Int. Dairy J. 5(8): 877. http://dx.doi.org/10.1016/0958-6946(95)00037-2.
Wood B.J.B. and Holzapfel W.H. 1995. The Genera of Lactic Acid Bacteria, p. 398-399. Blackie Academic and Professional, Glasgow.
Wouters J.T.M., Ayad E.H.E., Hugenholtz J. and Smit G. 2002. Microbes from raw milk for fermented dairy products. Int. Dairy J. 12(2-3): 91. http://dx.doi.org/10.1016/S0958-6946(01)00151-0.
Arahal D.R., Sánchez E., Macián M.C. and Garay E. 2008. Value of recN sequences for species identification and as a phylogenetic marker within the family “Leuconostocaceae”. Int. Microbiol. 11(1): 33. http://dx.doi.org/10.2436/20.1501.01.42.
Ashmaig A., Hasan A. and El Gaali E. 2009. Identification of lactic acid bacteria isolated from traditional Sudanese fermented camel’s milk (Gariss). Afr. J. Microbiol. Res. 3(8): 451.
Bendimerad N., Kihal M. and Berthier F. 2012. Isolation, identification, and technological characterization of wild leuconostocs and lactococci for traditional Raib type milk fermentation. Dairy Sci. Technol. 92(3): 249. http://dx.doi.org/10.1007/s13594-012-0063-8.
Boudjenah-Haroun S., Laleye C.L., Senoussi C., Moulti Mati F., Si Ahmed S. and Mati A. 2012. Coagulation of camel milk using dromedary gastric enzymes as a substitute of the commercial rennet. Am. J. Food Technol. 7(7): 409. http://dx.doi.org/10.3923/ajft.2012.409.419.
Buffa M., Guamis B., Saldo J. and Trujillo A.J. 2004. Changes in organic acids during ripening of cheeses made from raw, pasteurized or high-pressure-treated goats’ milk. Lebensm. Wiss. Technol. 37(2): 247. http://dx.doi.org/10.1016/j.lwt.2003.08.006.
Centeno J.A., Gaya P., Medina M. and Núñez M. 2002. Cross-inhibition among wild strains of Lactococcus lactis isolated from the same ecological niche. J. Food Protect. 65(1): 205.
Church F.C., Swaisgood H.E., Porter D.H. and Catignani G.L. 1983. Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J. Dairy Sci. 66(6): 1219. http://dx.doi.org/10.3168/jds.S0022-0302(83)81926-2.
Delgado F., González-Crespo J., Cava R. and Ramírez R. 2011. Formation of the aroma of a raw goat milk cheese during maturation analysed by SPME–GC–MS. Food Chem. 129(3): 1156. http://dx.doi.org/10.1016/j.foodchem.2011.05.096.
Drici H., Gilbert C., Kihal M. and Atlan D. 2010. Atypical citrate-fermenting Lactococcus lactis strains isolated from dromedary’s milk. J. Appl. Microbiol. 108(2): 647. http://dx.doi.org/10.1111/j.1365-2672.2009.04459.x.
Dutcosky S.D. 1996. “Sensory analysis of foods”. Ed. da Champagnat, Curitiba, Brasil.
El Soda M. and Desmazeaud M.J. 1982. Les peptides-hydrolases de lactobacilles du groupe Thermobacterium. 1. Mise en evidence de ces activites chez Lactobacillus helveticus, L. acidophilus, L. lactis et L. bulgaricus. Can. J. Microbiol. 28(10): 1181. http://dx.doi.org/10.1139/m82-174.
El Zubeir I.E.M. and Jabreel S.O. 2008. Fresh cheese from camel milk coagulated with Camifloc. Int. J. Dairy Technol. 61(1): 90. http://dx.doi.org/10.1111/j.1471-0307.2008.00360.x.
Engels W.J.M., Dekker R., De Jong C., Neeter R. and Visser S. 1997. A comparative study of volatile compounds in the water-soluble fraction of various types of ripened cheese. Int. Dairy J. 7(4): 255. http://dx.doi.org/10.1016/S0958-6946(97)00003-4.
FAO, 2008. Agro-statistics Database. Food and Agriculture Organization of the United Nations, Rome.
Farah Z. 1993. Composition and characteristics of camel milk. J. Dairy Res. 60(4): 603.
Farah Z. and Bachman M.R. 1987. Rennet coagulation properties of camel milk. Milchwissenschaft 42(11): 689.
Garabal J.I., Rodríguez-Alonso P. and Centeno J.A., 2008. Characterization of lactic acid bacteria isolated from raw cows’ milk cheeses currently produced in Galicia (NW Spain). LWT – Food Sci. Technol. 41(8): 1452. http://dx.doi.org/10.1016/j.lwt.2007.09.004.
González de Llano D., Rodríguez A. and Cuesta P. 1996. Effect of lactic starter cultures on the organic acid composition of milk and cheese during ripening–analysis by HPLC. J. Appl. Bacteriol. 80(5): 570. http://dx.doi.org/10.1111/j.1365-2672.1996.tb03259.x.
Herrero M., Mayo B., González B. and Suárez J.E. 1996. Evaluation of technologically important traits in lactic acid bacteria isolated from spontaneous fermentations. J. Appl. Bacteriol. 81(5): 565. http://dx.doi.org/10.1111/j.1365-2672.1996.tb03548.x.
Herreros M.A., Fresno J.M., González Prieto M.J. and Tornadijo M.E. 2003. Technological characterization of lactic acid bacteria isolated from Armada cheese (a Spanish goats’ milk cheese). Int. Dairy J. 13(6): 469. http://dx.doi.org/10.1016/S0958-6946(03)00054-2.
IDF, 1995. IDF guideline-determination of acidifying activity of dairy cultures. In: IDF Bulletin 306, p. 34-36. International Dairy Federation, Brussels.
IDF, 1997. Dairy starter cultures of lactic acid bacteria (LAB). Standard of identity. IDF Standard 149A. International Dairy Federation, Brussels.
Kaminarides S., Stamou P. and Massouras T. 2007. Changes of organic acids, volatile aroma compounds and sensory characteristics of Halloumi cheese kept in brine. Food Chem. 100(1): 219. http://dx.doi.org/10.1016/j.foodchem.2005.09.039.
Kondyli E., Massouras T., Katsiari M.C. and Voutsinas L.P. 2003. Free fatty acids and volatile compounds in low-fat Kefalograviera-type cheese made with commercial adjunct cultures. Int. Dairy J. 13(1): 47. http://dx.doi.org/10.1016/S0958-6946(02)00144-9.
Konuspayeva G., Faye B. and Loiseau G. 2009. The composition of camel milk: A meta-analysis of the literature data. J. Food Compos. Anal. 22(2): 95. http://dx.doi.org/10.1016/j.jfca.2008.09.008.
Limonet M., Cailliez-Grimal C., Linder M., Revol-Junelles A.M. and Millière J.B. 2004. Cell envelope analysis of insensitive, susceptible or resistant strains of Leuconostoc and Weissella genus to Leuconostoc mesenteroides FR 52 bacteriocins. FEMS Microbiol. Lett. 241(1): 49. http://dx.doi.org/10.1016/j.femsle.2004.10.002.
Lorenzo J.M. 2014. Influence of the type of fiber coating and extraction time on foal dry-cured loin volatile compounds extracted by solid-phase microextraction (SPME). Meat Sci. 96(1): 179. http://dx.doi.org/10.1016/j.meatsci.2013.06.017.
Lorenzo J.M. and Fonseca S. 2014. Volatile compounds of Celta dry-cured ‘lacón’ as affected by cross-breeding with Duroc and Landrace genotypes. J. Sci. Food Agr. 94(14): 2978. http://dx.doi.org/10.1002/jsfa.6643.
Macedo A.C., Vieira M., Poças R. and Malcata F.X. 2000. Peptide hydrolase system of lactic acid bacteria isolated from Serra da Estrela cheese. Int. Dairy J. 10(11): 769. http://dx.doi.org/10.1016/S0958-6946(00)00111-4.
Marco A., Navarro J.L. and Flores M. 2004. Volatile compounds of dry-fermented sausages as affected by solid-phase microextraction (SPME). Food Chem. 84(4): 633. http://dx.doi.org/10.1016/S0308-8146(03)00288-7.
McSweeney P.L.H. and Sousa M.J. 2000. Biochemical pathways for the production of flavor compounds in cheese during ripening: a review. Lait 80(3): 293. http://dx.doi.org/10.1051/lait:2000127.
Menéndez S., Centeno J.A., Godínez R. and Rodríguez-Otero J.L. 2000. Effect of Lactobacillus strains on the ripening and organoleptic characteristics of Arzúa-Ulloa cheese. Int. J. Food Microbiol. 59(1-2): 37. http://dx.doi.org/10.1016/S0168-1605(00)00286-5.
Nandan A., Gaurav A., Pandey A. and Madhavan Nampoothiri K. 2010. Arginine specific aminopeptidase from Lactobacillus brevis. Braz. Arch. Biol. Technol. 53(6): 1443. http://dx.doi.org/10.1590/S1516-89132010000600021.
Nickels C. and Leesment H. 1964. Method for the differentiation and qualitative determination of starter bacteria. Milchwissenschaft 19: 374.
Nieto-Arribas P., Seseña S., Poveda J.M., Palop L. and Cabezas L. 2009. Genotypic and technological characterization of Lactococcus lactis isolates involved in processing of artisanal Manchego cheese. J. Appl. Microbiol. 107(5): 1505. http://dx.doi.org/10.1111/j.1365-2672.2009.04334.x.
Nieto-Arribas P., Seseña S., Poveda J.M., Palop L. and Cabezas L. 2010. Genotypic and technological characterization of Leuconostoc isolates to be used as adjunct starters in Manchego cheese manufacture. Food Microbiol. 27(1): 85. http://dx.doi.org/10.1016/j.fm.2009.08.006.
Rodríguez-Alonso P., Garabal J.I. and Centeno J.A. 2008. Preliminary characterization of staphylococcal, micrococcal and yeast isolates obtained from raw cow milk cheeses currently produced in Galicia (NW Spain). Ital. J. Food Sci. 20(2): 161.
Settanni L. and Moschetti G. 2010. Non-starter lactic acid bacteria used to improve cheese quality and provide health benefits. Food Microbiol. 27(6): 691. http://dx.doi.org/10.1016/j.fm.2010.05.023.
Sreekumar R., Al-Attabi Z., Deeth H.C. and Turner M.S. 2009. Volatile sulfur compounds produced by probiotic bacteria in the presence of cysteine or methionine. Lett. Appl. Microbiol. 48(6): 777. http://dx.doi.org/10.1111/j.1472-765X.2009.02610.x.
Urbach G. 1995. Contribution of lactic acid bacteria to flavour compound formation in dairy products. Int. Dairy J. 5(8): 877. http://dx.doi.org/10.1016/0958-6946(95)00037-2.
Wood B.J.B. and Holzapfel W.H. 1995. The Genera of Lactic Acid Bacteria, p. 398-399. Blackie Academic and Professional, Glasgow.
Wouters J.T.M., Ayad E.H.E., Hugenholtz J. and Smit G. 2002. Microbes from raw milk for fermented dairy products. Int. Dairy J. 12(2-3): 91. http://dx.doi.org/10.1016/S0958-6946(01)00151-0.
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May 31, 2016
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Carballo, J. (2016). POTENTIAL TECHNOLOGICAL INTEREST OF INDIGENOUS LACTIC ACID BACTERIA FROM ALGERIAN CAMEL MILK. Italian Journal of Food Science, 28(4), 598-611. https://doi.org/10.14674/1120-1770/ijfs.v391
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Biografia autore
Javier Carballo, University of Vigo
Professor, Food Rechnology AreaCome citare
Carballo, J. (2016). POTENTIAL TECHNOLOGICAL INTEREST OF INDIGENOUS LACTIC ACID BACTERIA FROM ALGERIAN CAMEL MILK. Italian Journal of Food Science, 28(4), 598-611. https://doi.org/10.14674/1120-1770/ijfs.v391