Probiotic Potential of Autochthone Microbiota from São Jorge and Parmigiano-Reggiano Cheeses


For a long time, ripened cheeses have been officially recognized as having human health beneficial properties. However, to date only a few studies have investigated the complex microbiota of S?o Jorge and Parmigiano-Reggiano cheeses in order to identify microorganisms with probiotic potential. Hence, with the purpose of analyzing the probiotic potential of autochthone bacteria from S?o Jorge and Parmigiano-Reggiano cheeses, lactic acid bacteria isolated from both products were isolated and their direct biotic interaction against three bacteria found in the human intestine evaluated. From a total of 225 bacterial autochthone isolates, 67 had synergetic behavior with Bifidobacterium animalis , 34 had no synergetic behavior with Shigella dysenteriae and 33 had antagonistic activity with this human pathogen. Biochemical tests were used to identify these cheese isolates with probiotic potential. Lactobacillus paracasei subsp paracasei Lactobacillus arhamnosus were found in São Jorge cheese and Lactobacillus rhamnosus , Lactobacillus buchneri and Lactobacillus curvatus in the Parmigiano cheese. Overall, initial exploratory studies with São Jorge cheese seem to show a higher number of potential probiotic agents than those found in the Parmigiano-Reggiano cheese. However, in order to better understand the functional potential of this traditional Portuguese cheese, further confirmatory studies should be pursued.

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Dias, S. , Oliveira, M. , Semedo-Lemsaddek, T. and Bernardo, F. (2014) Probiotic Potential of Autochthone Microbiota from São Jorge and Parmigiano-Reggiano Cheeses. Food and Nutrition Sciences, 5, 1793-1799. doi: 10.4236/fns.2014.518193.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC) (2013) The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011. EFSA Journal, 11, 3129.
[2] Giraffa, G., Chanishvili, N. and Widyastuti, Y. (2010) Importance of Lactobacilli in Food and Feed Biotechnology. Research in Microbiology, 161, 480-487.
[3] Cruz, A.G., Buriti, F., Souza, C.H., Faria, J.A. and Saad, S.M. (2009) Probiotic Cheese: Health Benefits, Technological and Stability Aspects. Trends in Food Science Technology, 20, 344-354.
[4] Drago, L., Gismondo, M.R., Lombardi, A., Ha?n, C. and Gozzini, L. (1997) Inhibition of in Vitro Growth of Enteropathogens by New Lactobacillus Isolates of Human Intestinal Origin. FEMS Microbiology Letters, 153, 455-463.
[5] Firmesse, O., Alvaro, E., Mogenet, A., Bresson, J.L., Lemee, R., Le Ruyet, P. and Rigottier-Gois, L. (2008) Fate and Effects of Camembert Cheese Micro-Organisms in the Human Colonic Microbiota of Healthy Volunteers after Regular Camembert Consumption. International Journal of Food Microbiology, 125, 176-181.
[6] Gopal, P.K., Prasad, J., Smart, J. and Gill, H.S. (2001) In Vitro Adherence Properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 Strains and Their Antagonistic Activity against an Enterotoxigenic Escherichia coli. International Journal of Food Microbiology, 67, 207-216.
[7] Grimoud, J., Durand, H., Courtin, C., Monsan, P., Ouarne, F., Theodorou, V. and Roques, C. (2010) In Vitro Screening of Probiotic Lactic Acid Bacteria and Prebiotic Glucooligosaccharides to Select Effective Synbiotics. Anaerobe, 16, 493-500.
[8] Hosono, A., Otani, H., Yasui, H. and Watanuki, M. (2002) Impact of Fermented Milk on Human Health: Cholesterol-Lowering and Immunomodulatory Properties of Fermented Milk. Animal Science Journal, 73, 241-256.
[9] Morandi, S. and Brasca, M. (2012) Safety Aspects, Genetic Diversity and Technological Characterisation of Wild- Type Streptococcus thermophilus Strains Isolated from North Italian Traditional Cheeses. Food Control, 23, 203-209.
[10] Saarela, M., Mogense, G., Fondén, R., M?tt?, J. and Mattila-Sandholm, T. (2000) Probiotic Bacteria: Safety, Functional and Technological Properties. Journal of Biotechnology, 84, 197-215.
[11] Gareau, M.G., Sherman, P.M. and Walker, W.A. (2010) Probiotics and the Gut Microbiota in Intestinal Health and Di- sease. Nature Reviews Gastroenterology & Hepatology, 7, 503-514.
[12] De Filippis, F., La Storia, A., Stellato, G., Gatti, M. and Ercolini, D. (2014) A Selected Core Microbiome Drives the Early Stages of Three Popular Italian Cheese Manufactures. PLoS ONE, 9, e89680.
[13] Kongo, J.M., Ho, A.J., Malcata, F.X. and Wiedmann, M. (2007) Characterization of Dominant Lactic Acid Bacteria Isolated from S?o Jorge Cheese, Using Biochemical and Ribotyping Methods. Journal of Applied Microbiology, 103, 1838-1844.
[14] Neviani, E., Bottari, B., Lazzi, C. and Gatti, M. (2013) New Developments in the Study of the Microbiota of Raw-Milk, Long-Ripened Cheeses by Molecular Methods: The Case of Grana Padano and Parmigiano Reggiano. Frontiers in Mi- crobiology, Published Online.
[15] Solieri, L., Bianchi, A., Mottolese, G., Lemmetti, F. and Giudici, P. (2014) Tailoring the Probiotic Potential of Non- Starter Lactobacillus Strains from Ripened Parmigiano Reggiano Cheese by in Vitro Screening and Principal Component Analysis. Food Microbiology, 38, 240-249.
[16] Succi, M., Tremonte, P., Reale, A., Sorrentino, E., Grazia, L., Pacifico, S. and Coppola, R. (2005) Bile Salt and Acid Tolerance of Lactobacillus rhamnosus Strains Isolated from Parmigiano Reggiano Cheese. FEMS Microbiology Letters, 244, 129-137.
[17] Marteau, P.R., Vrese, M., Cellier, C.J. and Schrezenmeir, J. (2001) Protection from Gastrointestinal Diseases with the Use of Probiotics. American Journal of Clinical Nutrition, 73, 430-436
[18] World Health Organization (2014) Health Topics: Shigella.
[19] Fernandez, M.I. and Sansonetti, P.J. (2003) Shigella Interaction with Intestinal Epithelial Cells Determines the Innate Immune Response in Shigellosis. International Journal of Medical Microbiology, 293, 55-67.
[20] Russell, D.A., Ross, R.P., Fitzgerald, G.F. and Stanton, C. (2011) Metabolic Activities and Probiotic Potential of Bifidobacteria. International Journal of Food Microbiology, 149, 88-105.
[21] EFSA (2007) Introduction of a Qualified Presumption of Safety (QPS) Approach for Assessment of Selected Microorganisms Referred to EFSA. The EFSA Journal, 587, 1-16.
[22] FAO: Food and Agriculture Organization of the United Nations and World Health Organization (2002) Guidelines for the Evaluation of Probiotcs in Food. Joint FAO/WHO Working Group Report 2002, Ontario, p. 11.
[23] Lynch, C.M., Muir, D.D., Banks, J.M., McSweeney, P.L.H. and Fox, P.F. (1999) Influence of Adjunct Cultures of Lac- tobacillus paracasei ssp. paracasei or Lactobacillus plantarum on Cheddar Cheese Ripening. Journal of Dairy Science, 82, 1618-1628.
[24] Ong, L., Henriksson, A. and Shah, N.P. (2007) Proteolytic Pattern and Organic Acid Profiles of Probiotic Cheddar Cheese as Influenced by Probiotic Strains of Lactobacillus acidophilus, Lb. paracasei, Lb. casei or Bifidobacterium sp. International Dairy Journal, 17, 67-78.
[25] Beresford, T.P., Fitzsimons, N.A., Brenna, N.L. and Cogan, T.M. (2001) Recent Advances in Cheese Microbiology. International Dairy Journal, 11, 259-274.
[26] Lin, T.H. and Pan, T.M. (2011) Antimicrobial Activity of Metabolites Produced by Lactobacillus paracasei subsp. paracasei NTU 101 and Lactobacillus plantarum. NTU 102.
[27] Sa, A., Krishnaa, R.S., Pavithrab, V., Hemalathab, V. and Ingalea, P. (2011) Production and Antibacterial Activity of Bacteriocin by Lactobacillus paracasei Isolated from Donkey Milk. International Journal of Current Sciences, 109- 115.
[28] Tolinacki, M., Kojic, M., Lozo, J., Terzic-Vidojevic, A., Topisirovic, L. and Fira, D. (2010) Characterization of the Bacteriocin-Producing Strain Lactobacillus paracasei subsp. paracasei BGUB9. Archives of Biological Sciences, 62, 889-899.
[29] Pangsomboon, K., Bansal, S., Martin, G.P., Suntinanalert, P., Kaewnopparat, S. and Srichana, T. (2009) Further Characterization of a Bacteriocin Produced by Lactobacillus paracasei HL32. Journal of Applied Microbiology, 106, 1928-1940.
[30] Janheris, G., Vogelsang, H., Kiessling, G., Schubert, R., Bunte, C. and Hammes, W.P. (2002) Influence of Probiotic Sausage (Lactobacillus paracasei) on Blood Lipids and Immunological Parameters of Healthy Volunteers. Food Research International, 35, 133-138.
[31] Lee, J., Yun, H.S., Cho, K.W., Oh, S., Kim, S.H., Chun, T., Kim, B. and Whang, K.Y. (2011) Evaluation of Probiotic Characteristics of Newly Isolated Lactobacillus spp.: Immune Modulation and Longevity. International Journal of Food Microbiology, 148, 80-86.
[32] Forestier, C., De Champs, C., Vatoux, C. and Joly, B. (2001) Probiotic Activities of Lactobacillus caseirhamnosus: In Vitro Adherence to Intestinal Cells and Antimicrobial Properties. Research in Microbiology, 152, 167-173.
[33] Sarika, A.R., Lipton, A.P. and Aishwarya, M.S. (2010) Bacteriocin Production by a New Isolate of Lactobacillus rhamnosus GP1 under Different Culture Conditions. Advance Journal of Food Science and Technology, 2, 291-297.
[34] Collado, M.C., Meriluoto, J. and Salminen, S. (2007) In Vitro Analysis of Probiotic Strain Combinations to Inhibit Pathogen Adhesion to Human Intestinal Mucus. Food Research International, 40, 629-636.
[35] Gala, E., Landi, S., Solieri, L., Nocetti, M., Pulvirenti, A. and Giudici, P. (2008) Diversity of Lactic Acid Bacteria Po- pulation in Ripened Parmigiano Reggiano Cheese. International Journal of Food Microbiology, 125, 347-351.
[36] Liu, S., Skinner-Nemec, K.A. and Leathers, T.D. (2008) Lactobacillus buchneri Strain NRRL B-30929 Converts a Concentrated Mixture of Xylose and Glucose into Ethanol and Other Products. Journal of Industrial Microbiology & Biotechnology, 35, 75-81.
[37] Yildirim, Z. and Yildirim, M. (2001) Characterization of Buchnericin LB Produced by Lactobacillus buchneri. Turkish Journal of Biology, 25, 73-82.
[38] Zeng, X.Q., Pan, D.D. and Guo, Y.X. (2010) The Probiotic Properties of Lactobacillus buchneri P2. Journal of Applied Microbiology, 108, 2059-2066.
[39] Coppola, R., Nanni, M., Iorizzo, M., Sorrentino, A., Sorrentino, E., Chiavari, C. and Grazia, L. (2000) Microbiological Characteristics of Parmigiano Reggiano Cheese during the Cheesemaking and the First Months of the Ripening. Lait, 80, 479-490.
[40] Van Hoorde, K., Verstraete, T., Vandamme, P. and Huys, G. (2008) Diversity of Lactic Acid Bacteria in Two Flemish Artisan Raw Milk Gouda-Type Cheeses. Food Microbiology, 25, 929-935.
[41] 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.
[42] Tichaczek, P.S., Vogel, R. and Hammes, W.P. (1993) Cloning and Sequencing of Cur A Encoding Curvacin A, the Bacteriocin Produced by Lactobacillus curvatus LTH1174. Archives of Microbiology, 160, 279-283.
[43] Ghalfi, H., Thornart, P. and Benkerroum, N. (2006) Inhibitory Activity of Lactobacillus curvatus CWBI-B28 against Listeria monocytogenes and ST-Verotoxin Producing Eschericia coli O157. African Journal of Biotechnology, 5, 2303- 2306.
[44] Todorov, S.D., Furtado, D.N., Saad, S., Tome, E. and Franco, B.D.G.M. (2011) Potential Beneficial Proprieties of Bac- teriocin-Producing Lactic Acid Bacteria Isolated from Smoked Salmon. Journal of Applied Microbiology, 110, 971- 986.
[45] Basker, K., Reddy, P.K., Raghavendra, P., Kumar, B.G., Misra, M.C. and Prapulla, G. (2007) Screening of Probiotic Proprieties of Lactic Acid Bacteria Isolated from Kanjika, an Ayruvedic Lactic Acid Fermented Product: An In-Vitro Evaluation. Journal of General and Applied Microbiology, 53, 207-213.
[46] Nemeth, E., Fajdiga, S., Malago, J., Koninkx, J., Tooten, P. and van Dijk, J. (2006) Inhibition of Salmonella-Induced IL-8 Synthesis and Expression of Hsp70 in Enterocyte-Like Caco-2 Cells after Exposure to Non-Starter Lactobacilli. International Journal of Food Microbiology, 112, 266-274.

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