Effect of the addition of phytosterols and tocopherols on Streptococcus thermophilus robustness during industrial manufacture and ripening of a functional cheese as evaluated by qPCR and RT-qPCR
The quality of functional food products designed for the prevention of degenerative diseases can be affected by the incorporation of bioactive compounds. In many types of cheese, the performance of starter microorganisms is critical for optimal elaboration and for providing potential probiotic benef...
Guardado en:
| Autor principal: | |
|---|---|
| Otros Autores: | , , , , , , |
| Formato: | Capítulo de libro |
| Lenguaje: | Inglés |
| Publicado: |
Elsevier B.V.
2016
|
| Acceso en línea: | Registro en Scopus DOI Handle Registro en la Biblioteca Digital |
| Aporte de: | Registro referencial: Solicitar el recurso aquí |
| Sumario: | The quality of functional food products designed for the prevention of degenerative diseases can be affected by the incorporation of bioactive compounds. In many types of cheese, the performance of starter microorganisms is critical for optimal elaboration and for providing potential probiotic benefits. Phytosterols are plant lipophilic triterpenes that have been used for the design of functional dairy products because of their ability to lower serum cholesterol levels in humans. However, their effect on the starter culture behavior during cheesemaking has not yet been studied. Here, we followed DNA and RNA kinetics of the bacterium Streptococcus thermophilus, an extensively used dairy starter with probiotic potential, during industrial production of a functional, semi-soft, reduced-fat cheese containing phytosterol esters and alpha-tocopherol as bioactive compounds. For this purpose, real-time quantitative PCR (qPCR) and reverse transcription-qPCR (RT-qPCR) assays were optimized and applied to samples obtained during the manufacture and ripening of functional and control cheeses. An experimental set-up was used to evaluate the detection threshold of free nucleic acids for extraction protocols based on pelleted microorganisms. To our knowledge, this straight-forward approach provides the first experimental evidence indicating that DNA is not a reliable marker of cell integrity, whereas RNA may constitute a more accurate molecular signature to estimate both bacterial viability and metabolic activity. Compositional analysis revealed that the bioactive molecules were effectively incorporated into the cheese matrix, at levels considered optimal to exert their biological action. The starter S. thermophilus was detected by qPCR and RT-qPCR during cheese production at the industrial level, from at least 30 min after its inoculation until 81 days of ripening, supporting the possible role of this species in shaping organoleptic profiles. We also showed for the first time that the addition of phytosterols at functional concentrations, not only did not affect starter performance but also correlated with a significant increase in target DNA and cDNA levels in most of the time points evaluated throughout cheesemaking. Therefore, these findings suggest that the growth and metabolism of S. thermophilus may be enhanced by the incorporation of these biologically active molecules during cheese production, providing important information for the industrial design of novel fermented foods. © 2016 Elsevier B.V. |
|---|---|
| Bibliografía: | Achilleos, C., Berthier, F., Quantitative PCR for the specific quantification of Lactococcus lactis and Lactobacillus paracasei and its interest for Lactococcus lactis in cheese samples (2013) Food Microbiol., 36 (2), pp. 286-295 Agerholm-Larsen, L., Bell, M.L., Grunwald, G.K., Astrup, A., The effect of a probiotic milk product on plasma cholesterol: a meta-analysis of short-term intervention studies (2000) Eur. J. Clin. Nutr., 54 (11), pp. 856-860 Aldrete-Tapia, A., Escobar-Ramírez, M.C., Tamplin, M.L., Hernández-Iturriaga, M., High-throughput sequencing of microbial communities in Poro cheese, an artisanal Mexican cheese (2014) Food Microbiol., 44, pp. 136-141 Amaretti, A., di Nunzio, M., Pompei, A., Raimondi, S., Rossi, M., Bordoni, A., Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities (2013) Appl. Microbiol. Biotechnol., 97 (2), pp. 809-817 Angeles, A.G., Marth, E.H., Growth and activity of lactic-acid bacteria in soymilk. I: growth and acid production (1971) J. Milk Food Technol., 34, pp. 30-36 Código Alimentario Argentino (Art. 625). (2012), Ed. De La Canal & Asociados SRL, Buenos Aires, Argentina; Bennama, R., Fernández, M., Ladero, V., Alvarez, M.A., Rechidi-Sidhoum, N., Bensoltane, A., Isolation of an exopolysaccharide-producing Streptococcus thermophilus from Algerian raw cow milk (2012) Eur. Food Res. Technol., 234, pp. 119-125 Bruno-Bárcena, J.M., Azcárate-Peril, M.A., Hassan, H.M., Role of antioxidant enzymes in bacterial resistance to organic acids (2010) Appl. Environ. Microbiol., 76 (9), pp. 2747-2753 Carraro, L., Maifreni, M., Bartolomeoli, I., Martino, M.E., Novelli, E., Frigo, F., Marino, M., Cardazzo, B., Comparison of culture-dependent and -independent methods for bacterial community monitoring during Montasio cheese manufacturing (2011) Res. Microbiol., 162 (3), pp. 231-239 Chumchuere, S., Robinson, R.K., Selection of starter cultures for the fermentation of soya milk (1999) Food Microbiol., 16, pp. 129-137 Cocolin, L., Alessandria, V., Dolci, P., Gorra, R., Rantsiou, K., Culture independent methods to assess the diversity and dynamics of microbiota during food fermentation (2013) Int. J. Food Microbiol., 167 (1), pp. 29-43 De Pasquale, I., Di Cagno, R., Buchin, S., De Angelis, M., Gobbetti, M., Microbial ecology dynamics reveal a succession in the core microbiota involved in the ripening of pasta filata caciocavallo pugliese cheese (2014) Appl. Environ. Microbiol., 80 (19), pp. 6243-6255 Delcenserie, V., Taminiau, B., Delhalle, L., Nezer, C., Doyen, P., Crevecoeur, S., Roussey, D., Daube, G., Microbiota characterization of a Belgian protected designation of origin cheese, Herve cheese, using metagenomic analysis (2014) J. Dairy Sci., 97 (10), pp. 6046-6056 Delgado, S., Rachid, C.T., Fernández, E., Rychlik, T., Alegría, A., Peixoto, R.S., Mayo, B., Diversity of thermophilic bacteria in raw, pasteurized and selectively-cultured milk, as assessed by culturing, DGGE and pyrosequencing (2013) Food Microbiol., 36 (1), pp. 103-111 Desfossés-Foucault, É., LaPointe, G., Roy, D., Dynamics and rRNA transcriptional activity of lactococci and lactobacilli during Cheddar cheese ripening (2013) Int. J. Food Microbiol., 166 (1), pp. 117-124 Di Marzio, L., Centi, C., Cinque, B., Masci, S., Giuliani, M., Arcieri, A., Zicari, L., Cifone, M.G., Effect of the lactic acid bacterium Streptococcus thermophilus on stratum corneum ceramid levels and signs and symptoms of atopic dermatitis patients (2003) Exp. Dermatol., 12 (5), pp. 615-620 Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W., Grupo InfoStat, FCA, Universidad Nacional de Córdoba (2015), http://www.infostat.com.ar, Argentina. (URL); Dolci, P., De Filippis, F., La Storia, A., Ercolini, D., Cocolin, L., RRNA-based monitoring of the microbiota involved in Fontina PDO cheese production in relation to different stages of cow lactation (2014) Int. J. Food Microbiol., 185, pp. 127-135 Falentin, H., Henaff, N., Le Bivic, P., Deutsch, S.M., Parayre, S., Richoux, R., Sohier, D., Postollec, F., Reverse transcription quantitative PCR revealed persistency of thermophilic lactic acid bacteria metabolic activity until the end of the ripening of Emmental cheese (2012) Food Microbiol., 29, pp. 132-140 Farnworth, E.R., Mainville, I., Desjardins, M.P., Gardner, N., Fliss, I., Champagne, C., Growth of probiotic bacteria and bifidobacteria in a soy yogurt formulation (2007) Int. J. Food Microbiol., 116, pp. 174-181 Folch, J., Lees, M., Stanley, G.H.S., A simple method for the isolation and purification of total lipids from animal tissues (1957) J. Biol. Chem., 226, pp. 497-509 Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H., (2000) Fundamentals of Cheese Science, , AN Aspen Publishers Inc., Gaithersburg, Ma., USA Fox, P.F., McSweeney, P.L., Cogan, T.M., Guinee, T.P., (2004) Cheese: Chemistry, Physics and Microbiology: General Aspects, 3rd Ed, 1. , Elsevier Academic, Oxford, United Kingdom García, P.T., Pensel, N.A., Sancho, A.M., Latimori, N.J., Kloster, A.M., Amigone, M.A., Casal, J.J., Beef lipids in relation to animal breed and nutrition in Argentina (2008) Meat Sci., 79, pp. 500-508 Gatti, M., Bottari, B., Lazzi, C., Neviani, E., Mucchetti, G., Invited review: microbial evolution in raw-milk, long-ripened cheeses produced using undefined natural whey starters (2014) J. Dairy Sci., 2, pp. 573-591 Gluck, U., Gebbers, J.O., Ingested probiotics reduce nasal colonization with pathogenic bacteria (Staphylococcus aureus, Streptococcus pneumonia and β haemolytic streptococci) (2003) Am. J. Clin. Nutr., 77 (2), pp. 517-520 Hickson, M., D'Souza, A.L., Muthu, N., Rogers, T.R., Want, S., Rajkumar, C., Bulpitt, C.J., Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial (2007) Br. Med. J., 335 (7610), p. 80 Food and nutrition board (2000) Dietary Reference Intakes: Vitamin C, Vitamin E, Selenium and Carotenoids, , National Academy Press, Washington DC (2004) ISO 5534/IDF 4:2004: Reference Method for the Determination of the total Solids Content of Cheese and Processed Cheese (2006) ISO 5943/IDF 88:2006: Potentiometric Titration Method for the Determination of the Chloride Content of Cheese and Processed Cheese Products (2008) ISO 3433/IDF 222:2008: Van Gulik Method for the Determination of the Fat Content, as a Mass Fraction, of Cheese Irlinger, F., Mounier, J., Microbial interactions in cheese: implications for cheese quality and safety (2009) Curr. Opin. Biotechnol., 20, pp. 142-148 Jany, J.L., Barbier, G., Culture-independent methods for identifying microbial communities in cheese (2008) Food Microbiol., 25, pp. 839-848 Karleskind, D., Laye, I., Halpin, E., Morr, C.V., Improving acid production in soy-based yogurt by adding cheese whey proteins and mineral salts (1991) J. Food Sci., 56, pp. 999-1001 Lichtenstein, A.H., Wylie-Rosett, J., Diet and lifestyle recommendations revision 2006. A scientific statement from the American Heart Association Nutrition Committee (2006) Circulation, 114, pp. 82-96 Martirosyan, D.M., (2011) Introduction to Functional Food Science, , Food Science Publisher Masoud, W., Takamiya, M., Vogensen, F.K., Lillevang, S., Abu Al-Soud, W., Sørensen, S.J., Jakobsen, Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing (2011) Int. Dairy J., 21, pp. 142-148 Masoud, W., Vogensen, F.K., Lillevang, S., Abu Al-Soud, W., Sørensen, S.J., Jakobsen, M., The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR (2012) Int. J. Food Microbiol., 153 (1-2), pp. 192-202 Monu, E., Blank, G., Holley, R., Zawistowski, J., Phytosterols effects on milk and yogurt microflora (2008) J. Food Sci., 73 (3), pp. M121-M126 Mora, D., Arioli, S., Microbial urease in health and disease (2014) PloS One Pathogens, 10 (12) Mora, D., Monnet, C., Parini, C., Guglielmetti, S., Mariani, A., Pintus, P., Molinari, F., Manachini, P.L., Urease biogenesis in Streptococcus thermophilus (2005) Res. Microbiol., 156 (9), pp. 897-903 Rondanelli, M., Monteferrario, F., Faliva, M.A., Perna, S., Antoniello, N., Key points for maximum effectiveness and safety for cholesterol-lowering properties of plant sterols and use in the treatment of metabolic syndrome (2013) J. Sci. Food Agric., 93, pp. 2605-2610 Rossetti, L., Langman, L., Grigioni, G.M., Biolatto, A., Sancho, A.M., Comerón, E., Descalzo, A.M., Antioxidant status and odor profile in milk from silage or alfalfa-fed cows (2010) Aust. J. Dairy Technol., 65 (1), pp. 3-9 Ruggirello, M., Dolci, P., Cocolin, L., Detection and viability of Lactococcus lactis throughout cheese ripening (2014) PLoS One, 9 (12) Saavedra, J.M., Bauman, N.A., Perman, J.A., Yolken, R.H., Oung, I., Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus (1994) Lancet, 344, pp. 1046-1049 Shori, A.B., Antioxidant activity and viability of lactic acid bacteria in soybean-yogurt made from cow and camel milk (2013) J. Taibah Univ. Sci., 7, pp. 202-208 Sohier, D., Pavan, S., Riou, A., Combrisson, J., Postollec, F., Evolution of microbial analytical methods for dairy industry needs (2014) Front. Microbiol., 5, p. 16 Slavin, M., Yu, L.L., A single extraction and HPLC procedure for simultaneous analysis of phytosterols, tocopherols and lutein in soybeans (2012) Food Chem., 135 (4), pp. 2789-2795 Stevens, K.A., Jaykus, L.A., Direct detection of bacterial pathogens in representative dairy products using a combined bacterial concentration-PCR approach (2004) J. Appl. Microbiol., 97, pp. 1115-1122 van de Bunt, B., Bron, P.A., Sijtsma, L., de Vos, W.M., Hugenholtz, J., Use of non-growing Lactococcus lactis cell suspensions for production of volatile metabolites with direct relevance for flavor formation during dairy fermentations (2014) Microb. Cell Factories, 13, p. 176 |
| ISSN: | 01681605 |
| DOI: | 10.1016/j.ijfoodmicro.2016.06.003 |