Lactic acid microbiota identification in water, raw milk, endogenous starter culture, and fresh Minas artisanal cheese from the Campo das Vertentes region of Brazil during the dry and rainy seasons

Journal of Dairy Science

Volumn 99, Issue 8, 2016, Pages 6086-6096

  Castro, R D ^a   Oliveira, L G ^a   Sant'Anna, F M ^a   Luiz, L M P ^a   Sandes, S H C ^a   Silva, C I F ^a   Silva, A M ^b   Nunes, A C ^a   Penna, C F A M ^a   Souza, M R ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO JOÃO DEL REI   (Brazil)

Author keywords

16S rRNA sequencing; artisanal cheese; cheese composition; microbiology

Indexed keywords

LACTIC ACID; RAIN; WATER;

ANALYSIS; ANIMAL; BRAZIL; CHEESE; ENTEROCOCCUS; FOOD CONTROL; ISOLATION AND PURIFICATION; LACTOBACILLACEAE; LACTOBACILLALES; LACTOBACILLUS PLANTARUM; LACTOCOCCUS LACTIS; MICROBIOLOGY; MICROFLORA; MILK; SEASON;

ANIMALS; BRAZIL; CHEESE; ENTEROCOCCUS; FOOD MICROBIOLOGY; LACTIC ACID; LACTOBACILLACEAE; LACTOBACILLALES; LACTOBACILLUS PLANTARUM; LACTOCOCCUS LACTIS; MICROBIOTA; MILK; RAIN; SEASONS; WATER; WATER MICROBIOLOGY;

EID: 84973459093     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2015-10579     Document Type: Article

References (68)

1. Abriouel, H., Martín-Platero, A., Maqueda, M., Valdivia, E., Martínez-Bueno, M., Biodiversity of the microbial community in a Spanish farmhouse cheese as revealed by culture-dependent and culture-independent methods. Int. J. Food Microbiol. 127 (2008), 200–208.
2. Alegría, A., Alvarez-Martín, P., Sacristán, N., Fernández, E., Delgado, S., Mayo, B., Diversity and evolution of the microbial populations during manufacture and ripening of Casín, a traditional Spanish, starter-free cheese made from cow's milk. Int. J. Food Microbiol. 136 (2009), 44–51.
3. Andrews, W.H., Flowers, R.S., Silliker, J., Bailey, J.S., Salmonella. Downes, F.P., Ito, K., (eds.) Compendium of Methods for the Microbiological Examination of Foods, 4th, 2001, Am. Public Health Assoc., Washington, DC, 357–376.
4. Andrighetto, C., Knijff, E., Lombardi, A., Torriani, S., Vancanneyt, M., Kersters, K., Swings, J., Dellaglio, F., Phenotypic and genetic diversity of enterococci isolated from Italian cheeses. J. Dairy Res. 68 (2001), 303–316.
5. American Public Health Association. Eaton, A.D., Clesceri, L.S., Rice, E.W., Greenberg, A.E., (eds.) Standard Methods for the Examination of Water and Wastewater, 21st, 2005, Am. Public Health Assoc., Washington, DC.
6. Borelli, B.M., Ferreira, E.G., Lacerda, I.C.A., Santos, D.A., Carmo, L.S., Dias, R.S., Silva, M.C.C., Rosa, C.A., Enterotoxigenic Staphylococcus spp. and other microbial contaminants during production of Canastra cheese. Braz. J. Microbiol. 37 (2006), 545–550.
7. Brasil, Ministério da Saúde, Gabinete do Ministro. 2012. Portaria n. 2.914, de 12 de dezembro de 2011. Dispõe sobre procedimentos de controle e de vigilância da qualidade da água para consumo humano e seu padrão de potabilidade. Pages 43–49 in Diário Oficial da República Federativa do Brasil, Brasília, DF, Seção 1, 04 de janeiro de 2012. Ministério da Saúde, Brasilia, Brazil.
8. British Standards. Methods for chemical analysis of cheese. Determination of pH value. BS 770: Part 5, 1976, British Standards Institute, London, UK.
9. Chaves, A.H., Pinheiro, A.J.R., Teixeira, M.A., Isolamento, caracterização e identificação de bactérias do gênero Leuconostoc. Rev. Inst. Laticínios Cândido Tostes 50 (1995), 35–41.
10. Coppola, S., Fusco, V., Andolfi, R., Aponte, M., Blaiotta, G., Ercolini, D., Moschetti, G., Evaluation of microbial diversity during the manufacture of Fior di Latte di Agerola, a traditional raw milk pasta-filata cheese of the Naples area. J. Dairy Res. 73 (2006), 264–272.
11. Coppola, S., Parente, E., Dumontet, S., La Peccerella, A., The microflora of natural whey cultures utilized as starters in the manufacture of Mozzarella cheese from water-buffalo milk. Lait 68 (1988), 295–309.
12. Costa, G.M., Paiva, L.V., Figueiredo, H.C.P., Figueira, A.R., Pereira, U.P., Silva, N., Population diversity of Staphylococcus aureus isolates from bovine mastitis in Brazilian dairy herds. Res. Vet. Sci. 93 (2012), 733–735.
13. Dores, M.T., Nóbrega, J.E., Ferreira, C.L.L.F., Room temperature aging to guarantee microbiological safety of Brazilian artisan Canastra cheese. Food Sci. Technol. (Campinas) 33 (2013), 180–185.
14. Ercan, D., Korel, F., Orşahin, H., Microbiological quality of artisanal Sepet cheese. Int. J. Dairy Technol. 67 (2014), 384–393.
15. Feutry, F., Oneca, M., Berthier, F., Torre, P., Biodiversity and growth dynamics of lactic acid bacteria in artisanal PDO Ossau-Iraty cheeses made from raw ewe's milk with different starters. Food Microbiol. 29 (2012), 33–42.
16. Fontán, M.C.G., Franco, I., Prieto, B., Tornadijo, M.E., Carballo, J., Microbiological changes in ‘San Simón’ cheese throughout ripening and its relationship with physico-chemical parameters. Food Microbiol. 18 (2001), 25–33.
17. Guo, Y., Wang, L., Zou, Y., Xu, X., Li, S., Cao, Z., Changes in ruminal fermentation, milk performance and milk fatty acid profile in dairy cows with subacute ruminal acidosis and its regulation with pelleted beet pulp. Arch. Anim. Nutr. 67 (2013), 433–447.
18. Hamed, E., Elattar, A., Identification and some probiotic potential of lactic acid bacteria isolated from Egyptian camels milk. Life Sci. 10 (2013), 1952–1961.
19. Hammad, A.M., Hassan, H.A., Shimamoto, T., Prevalence, antibiotic resistance and virulence of Enterococcus spp. in Egyptian fresh raw milk cheese. Food Contr. 50 (2015), 815–820.
20. Instituto Brasileiro de Geografia e Estatística. Produção da Pecuária Municipal, 2011, Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro, Brazil.
21. IDF (International Dairy Federation). Cheese and processed cheese: Determination of total solids content. IDF Standard 4A, 1982, Int. Dairy Fed., Brussels, Belgium.
22. IDF (International Dairy Federation). Yogurt: Enumeration of characteristic microorganisms colony count technique at 37°C. IDF Standard 117A, 1988, Int. Dairy Fed., Brussels, Belgium.
23. IDF (International Dairy Federation). Milk: Determination of nitrogen content. IDF Standard 20B, 1993, Int. Dairy Fed., Brussels, Belgium.
24. IDF (International Dairy Federation). Milk: Enumeration of somatic cells. IDF Standard 148A, 1995, Int. Dairy Fed., Brussels, Belgium.
25. IDF (International Dairy Federation). Whole milk: Determination of milkfat, protein and lactose contend. Guidance on the operation of mid-infrared instruments. IDF Standard 141C, 2000, Int. Dairy Fed., Brussels, Belgium.
26. IDF (International Dairy Federation). Cheese: Determination of fat content. Butyrometer for Van Gulik method. ISO Standard 3432. IDF Standard 221, 2008, Int. Dairy Fed., Brussels, Belgium.
27. Instituto Nacional de Meteorologia. 2013a. Chuva acumulada mensal x nº de dias com chuva-Barbacena (MG)—para o ano: 2013. Accessed Dec. 10, 2014. http://www.inmet.gov.br/portal/index.php?r=tempo/graficos.
28. b Instituto Nacional de Meteorologia. 2013b. Temperaturas diárias (máxima, média, mínima)—Estação Barbacena (MG) 12/2013. Accessed Dec. 10, 2014. http://www.inmet.gov.br/portal/index.php?r=tempo/graficos.
29. 2014a Instituto Nacional de Meteorologia. 2014a. Chuva acumulada mensal x nº de dias com chuva-Barbacena (MG)—para o ano: 2014 até 22/12/2014. Accessed Dec. 10, 2014. http://www.inmet.gov.br/portal/index.php?r=tempo/graficos.
30. b Instituto Nacional de Meteorologia. 2014b. Temperaturas diárias (máxima, média, mínima)—Estação Barbacena (MG) 04/2014. Accessed Dec. 10, 2014. http://www.inmet.gov.br/portal/index.php?r=tempo/graficos.
31. Instituto Do Patrimônio Histórico e Artístico Nacional. 2008. Livro de Registro de Saberes. Brasília, DF. Accessed Dec. 29, 2014. http://www.iphan.gov.br/bcrE/pages/folProcessoRegistroE.jsf.
32. Jay, J.M., Loessner, M.J., Golden, D.D., Modern Food Microbiology, 7th, 2005, Springer, New York, NY.
33. Johler, S., Giannini, P., Jermini, M., Hummerjohann, J., Baumgartner, A., Stephan, R., Further evidence for staphylococcal food poisoning outbreaks caused by egc-encoded enterotoxins. Toxins (Basel) 7 (2015), 997–1004.
34. Kirmaci, H.A., Hayaloğ lu, A.A., Özer, H.B., Atasoy, A.F., Türkoğ lu, H., Evolution of proteolysis in Urfa cheese made from ewe's milk by wild type starter culture systems. Small Rumin. Res. 119 (2014), 120–129.
35. Kornacki, J.L., Johnson, J.L., Enterobacteriaceae, coliforms and Escherichia coli as quality and safety indicators. Downes, F.P., Ito, K., (eds.) Compendium of Methods for the Microbiological Examination of Foods, 4th, 2001, American Public Health Association, Washington, DC, 69–80.
36. Lancette, G.A., Tatini, S.R., Staphylococcus aureus. Downes, F.P., Ito, K., (eds.) Compendium of Methods for the Microbiological Examination of Foods, 4th, 2001, American Public Health Association, Washington, DC, 387–400.
37. Lane, D.J., 16S/23S rRNA sequencing. Stackebrandt, E., Goodfellow, M., (eds.) Nucleic Acid Techniques in Bacterial Systematics, 1991, Wiley, Chichester, UK, 115–175.
38. Lerch, S., Pires, J.A., Delavaud, C., Shingfield, K.J., Pomiès, D., Martin, B., Chilliard, Y., Ferlay, A., Rapeseed or linseed in dairy cow diets over 2 consecutive lactations: effects on adipose fatty acid profile and carry-over effects on milk fat composition in subsequent early lactation. J. Dairy Sci. 98 (2015), 1005–1018.
39. Lima, C.D.L.C., Lima, L.A., Cerqueira, M.M.O.P., Ferreira, E.G., Rosa, C.A., Bactérias do acido láctico e leveduras associadas com o queijo-de-minas artesanal produzido na região da Serra do Salitre, Minas Gerais. Arq. Bras. Med. Vet. Zootec. 61 (2009), 266–272.
40. MacFaddin, J.F., Biochemical Tests for Identification of Medical Bacteria, 2nd, 1980, Williams & Wilkins, Baltimore, MD.
41. Martins, J.M., Galinari, E., Pimentel Filho, N.J., Ribeiro Jr, J.I., Furtado, M.M., Ferreira, C.L.L.F., Determining the minimum ripening time of artisanal Minas cheese, a traditional Brazilian cheese. Braz. J. Microbiol. 46 (2015), 219–230.
42. Merck. 1993. Reactivos, Diagnóstica, Productos Químicos 1992/93. Merck, Darmstadt, Germany.
43. Minas Gerais. 2009. Instituto Mineiro de Agropecuária. Portaria n. 1022 de 3 nov. 2009. Identifica a região de Campo das Vertentes. Accessed Dec. 5, 2014. http://imanet.ima.mg.gov.br/nova/legis/portarias_pdf/1022.pdf.
44. Moreira, J.L.S., Mota, R.M., Horta, M.F., Teixeira, S.M.R., Neumann, E., Nicoli, J.R., Nunes, A.C., Identification to the species level of Lactobacillus isolated in probiotic prospecting studies of human, animal or food origin by 16S–23S rRNA restriction profiling. BMC Microbiol., 5, 2005, 15.
45. Morton, R.D., Aerobic plate count. Downes, F.P., Ito, K., (eds.) Compendium of Methods for the Microbiological Examination of Foods, 4th, 2001, American Public Health Association, Washington, DC, 63–67.
46. Murray, B.E., The life and times of the Enterococcus. Clin. Microbiol. Rev. 3 (1990), 46–65.
47. Nieto-Arribas, P., Seseña, S., Poveda, J.M., Palop, L., Cabezas, L., Genotypic and technological characterization of Leuconostoc isolates to be used as adjunct starters in Manchego cheese manufacture. Food Microbiol. 27 (2010), 85–93.
48. Oliveira, D.F., Porto, M.A.C., Bravo, C.E.C., Tonial, I.B., Caracterização físico-química de queijos Minas Artesanal produzidos em diferentes microrregiões de Minas Gerais. Rev. Bras. Econ. Domést. 24 (2013), 185–196.
49. de Paula, A.T., Jeronymo-Ceneviva, A.B., Silva, L.F., Todorov, S.D., Franco, B.D.G.M., Penna, A.L.B., Leuconostoc mesenteroides SJRP55: A potential probiotic strain isolated from Brazilian water buffalo mozzarella cheese. Probiotics Antimicrob. Proteins 6 (2014), 186–197.
50. Phillips, M., Kailasapathy, K., Tran, L., Viability of commercial probiotic cultures (L. acidophilus, Bifidobacterium sp., L. casei, L. paracasei and L. rhamnosus) in cheddar cheese. Int. J. Food Microbiol. 108 (2006), 276–280.
51. Ramirez-Chavarin, M.L., Wacher, C., Eslava-Campos, C.A., Perez- Chabela, M.L., Probiotic potential of thermotolerant lactic acid bacteria strains isolated from cooked meat products. Int. Food Res. J. 20 (2013), 991–1000.
52. Resende, M.F.S., Costa, H.H.S., Andrade, E.H.P., Acúrcio, L.B., Drummond, A.F., Cunha, A.F., Nunes, A.C., Moreira, J.L.S., Penna, C.F.A.M., Souza, M.R., Queijo-de-minas artesanal da Serra da Canastra: Influência da altitude das queijarias nas populações de bactérias ácido-lácticas. Arq. Bras. Med. Vet. Zootec. 63 (2011), 1532–1538.
53. Reysenbach, A.L., Longnecker, K., Kirshtein, J., Novel bacterial and archael lineages from an in situ growth chamber deployed at a mid-Atlantic ridge hydrothermal vent. Appl. Environ. Microbiol. 66 (2000), 3798–3806.
54. Sandes, S.H., Alvin, L.B., Silva, B.C., Zanirati, D.F., Jung, L.R., Nicoli, J.R., Neumann, E., Nunes, A.C., Lactobacillus species identification by amplified ribosomal 16S–23S rRNA restriction fragment length polymorphism analysis. Benef. Microbes 5 (2014), 471–481.
55. Scott, R., Fabricación de Queso, 2nd, 2002, Editora Acribia S. A., Zaragoza, Spain.
56. Silvetti, T., Morandi, S., Brasca, M., Biopreservation potential of Enterococcus faecalis isolated from Italian traditional raw milk cheeses. CyTA J. Food 12 (2014), 210–217.
57. Souza, C.F.V., Rosa, T.D., Ayub, M.A.Z., Changes in microbiological and physicochemical characteristics of Serrano cheese during manufacturing and ripening. Braz. J. Microbiol. 34 (2003), 260–266.
58. Stamford, T.L.M., Silva, C.G.M., Mota, R.A., Cunha Neto, A., Enterotoxidade de Staphylococcus spp. isolados de leite in natura. Ciênc. Tecnol. Aliment. 26 (2006), 41–45.
59. Suhren, G., Walte, H.G., First experiences with automatic flow cytometric determination of total bacteria count in raw milk. Bulletin of the International Dairy Federation (IDF). No. 358, 2000, 36–48.
60. Terzic-Vidojevic, A., Tolinacki, M., Nikolic, M., Lozo, J., Bejovic, J., Gulahmadov, S.G.O., Kuliev, A.A., Dalgalarrondo, M., Chobert, J.-M., Haertlé, T., Topisirovic, L., Phenotypic and genotypic characterization of lactic acid bacteria isolated from Azerbaijani traditional dairy products. Afr. J. Biotechnol. 8 (2009), 2576–2588.
61. Torriani, S., Felis, G.E., Dellaglio, F., Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA gene-derived primers. Appl. Environ. Microbiol. 67 (2001), 3450–3454.
62. Tournas, V., Stack, M.E., Mislivec, P.B., Koch, H.A., Bandler, R., Yeasts, molds and mycotoxins. Chapter 18 in Bacteriological Analytical Manual Online, 8th, 2001, United States Food and Drug Administration, Rockville, MD.
63. Veljovic, K., Terzic-Vidojevic, A., Vukasinovic, M., Strahinic, I., Begovic, J., Lozo, J., Ostojic, M., Topisirovic, L., Preliminary characterization of lactic acid bacteria isolated from Zlatar cheese. J. Appl. Microbiol. 103 (2007), 2142–2152.
64. Ward, L.J.H., Timmins, M.J., Differentiation of Lactobacillus casei, Lactobacillus paracasei and Lactobacillus rhamnosus by polymerase chain reaction. Lett. Appl. Microbiol. 29 (1999), 90–92.
65. Wattiaux, M. A. 2012. Composição do leite e seu valor nutricional. Essenciais em Gado de Leite (19), 73–76. Instituto Babcock para Pesquisa e Desenvolvimento da Pecuária Leiteira Internacional, University of Wisconsin-Madison. Accessed Dec. 5, 2014. http://babcock.wisc.edu/sites/default/files/de/pt/de_19.pt.pdf.
66. WHO (World Health Organization). 2011a. Guidelines for drinking-water quality. 4th ed. Accessed Dec. 02, 2014. http://www.who.int/water_sanitation_health/publications/2011/dwq_chapters/en/index.html.
67. WHO (World Health Organization). 2011b. Hardness in drinking water. Background document for development of WHO Guidelines for drinking-water quality. Accessed Dec. 2, 2014. http://www.who.int/water_sanitation_health/dwq/chemicals/hardness.pdf.
68. Zahedi, F., Nasrabadi, M.H., Ebrahimi, M.T., Shabani, M., Aboutalebi, H., Study the effect of Lactobacillus brevis isolated from Iranian traditional cheese on cutaneous wound healing in male rats on days 3 and 14. Razi J. Med. Sci. 18 (2011), 16–23.