Screening of Lactobacillus strains for their ability to produce conjugated linoleic acid in milk and to adhere to the intestinal tract

Journal of Dairy Science

Volumn 98, Issue 10, 2015, Pages 6651-6659

  Sosa Castaneda J ^a   Hernandez Mendoza A ^a   Astiazaran Garcia H ^a   Garcia, H S ^b   Estrada Montoya, M C ^a   Gonzalez Cordova A F ^a   Vallejo Cordoba, B ^a  

^a CENTRO DE INVESTIGACIÓN EN ALIMENTACIÓN Y DESARROLLO   (Mexico)

^b INSTITUTO TECNOLÓGICO DE VERACRUZ   (Mexico)

Author keywords

Conjugated linoleic acid; Fermented milk; Lactic acid bacteria; Lactobacillus

Indexed keywords

CONJUGATED LINOLEIC ACID;

ANIMAL; BACTERIUM ADHERENCE; CHEMISTRY; DAIRY PRODUCT; FERMENTATION; GENETICS; LACTOBACILLUS; MALE; METABOLISM; MICROBIOLOGY; MILK; PHYSIOLOGY; RANDOMIZATION; RAT; SMALL INTESTINE; WISTAR RAT;

ANIMALS; BACTERIAL ADHESION; CULTURED MILK PRODUCTS; FERMENTATION; INTESTINE, SMALL; LACTOBACILLUS; LINOLEIC ACIDS, CONJUGATED; MALE; MILK; RANDOM ALLOCATION; RATS; RATS, WISTAR;

EID: 84942553984     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2014-8515     Document Type: Article

References (60)

1. Abd El-Salam M.H., El-Shafei K., Sharaf O.M., Effat B.A., Asem F.M., El-Aasar M. Screening of some potentially probiotic lactic acid bacteria for their ability to synthesis conjugated linoleic acid. Int. J. Dairy Technol. 2010, 63:62-69.
2. Alonso L., Cuesta E.P., Gilliland S.E. Production of free conjugated linoleic acid by Lactobacillus acidophilus and Lactobacillus casei of human intestinal origin. J. Dairy Sci. 2003, 86:1941-1946.
3. Andrade J.C., Ascencao K., Gullon P., Henriques S.M.S., Pinto J.M.S., Rocha-Santos T.A.P., Freitas A.C., Gomes A.M. Production of conjugated linoleic acid by food-grade bacteria: A review. Int. J. Dairy Technol. 2012, 65:467-481.
4. Bao Y., Zhang Y., Zhang Y., Liu Y., Wang S., Dong X., Wang Y., Zhang H. Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Contr. 2010, 21:695-701.
5. Begley M., Gahan C.G.M., Hill C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 2005, 29:625-651.
6. Benchaar C., Romero-Perez G.A., Chouinard P.Y., Hassanat F., Eugene M., Petit H.V., Cortes C. Supplementation of increasing amounts of linseed oil to dairy cows fed total mixed rations: Effects on digestion, ruminal fermentation characteristics, protozoal populations, and milk fatty acid composition. J. Dairy Sci. 2012, 95:4578-4590.
7. Bhattacharya A., Banu J., Rahman M., Causey J., Fernandes G. Biological effects of conjugated linoleic acids in health and disease. J. Nutr. Biochem. 2006, 17:789-810.
8. Bouzaine T., Dauphin R.D., Thonart Ph., Urdaci M.C., Hamdi M. Adherence and colonization properties of Lactobacillus rhamnosus TB1, a broiler chicken isolate. Lett. Appl. Microbiol. 2005, 40:391-396.
9. Chin S.F., Liu W., Storkson J.M., Ha Y.L., Pariza M.W. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J. Food Compos. Anal. 1992, 5:185-197.
10. Chouinard P.Y., Corneau L., Butler W.R., Chilliard Y., Drackley J.K., Bauman D.E. Effect of dietary lipid source on conjugated linoleic acid concentrations in milk fat. J. Dairy Sci. 2001, 84:680-690.
11. Correia M., Michel V., Matos A.A., Carvalho P., Oliveira M.J., Ferreira R.M., Dillies M.-A., Huerre M., Seruca R., Figueiredo C., Machado J.C., Touati E. Docosahexaenoic acid inhibits Helicobacter pylori growth in vitro and mice gastric mucosa colonization. PLoS ONE 2012, 7:e35072. http://dx.doi.org/10.1371/journal.pone.0035072.
12. do Espirito Santo A.P., Cartolano N.S., Silva T.F., Soares F.A., Gioielli L.A., Perego P., Converti A., Oliveira M.N. Fibers from fruit by-products enhance probiotic viability and fatty acid profile and increase CLA content in yoghurts. Int. J. Food Microbiol. 2012, 154:135-144.
13. Domagała J., Sady M., Najgebauer-Lejko D., Czernicka M., Wieteska I. The content of conjugated linoleic acid (CLA) in cream fermented using different starter cultures. Biotech. Anim. Husbandry 2009, 25:745-751.
14. Duangjitcharoen Y., Kantachote D., Ongsakul M., Poosaran N., Chaiyasut C. Potential use of probiotic Lactobacillus plantarum SS2 isolated from a fermented plant beverage: Safety assessment and persistence in the murine gastrointestinal tract. World J. Microbiol. Biotechnol. 2009, 25:315-321.
15. Farmani J., Safari M., Roohvand F., Razavi S.H., Aghasadeghi M.R., Noorbazargan H. Conjugated linoleic acid-producing enzymes: A bioinformatics study. Eur. J. Lipid Sci. Technol. 2010, 112:1088-1100.
16. Fernández de Palencia P., López P., Corbí A., Peláez C., Requena T. Probiotic strains: survival under simulated gastrointestinal conditions, in vitro adhesion to Caco-2 cells and effect on cytokine secretion. Eur. Food Res. Technol. 2008, 227:1475-1484.
17. Florence A., Silva R., Santo A., Gioielli L., Tamime A., Oliveira M. Increased CLA content in organic milk fermented by Bifidobacteria or yoghurt cultures. Dairy Sci. Technol. 2009, 89:541-553.
18. Flowers G., Ibrahim S.A., AbuGhazaleh A.A. Milk fatty acid composition of grazing dairy cows when supplemented with linseed oil. J. Dairy Sci. 2008, 91:722-730.
19. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226:497-509.
20. Fritsche J., Steinhart H. Amounts of conjugated linoleic acid (CLA) in German foods and evaluation of daily intake. Z. Lebensm. Unters. Forsch. 1998, 206:77-82.
21. Frizzo L.S., Soto L.P., Bertozzi E., Sequeira G., Marti L.E., Rosmini M.R. In vitro evaluation of the microbial probiotic capacities focused to design of multispecies probiotic inocula to be used in breeding of calves. Rev. Cienc. Vet. 2006, 5:69-81.
22. Fuller M.E., Streger S.H., Rothmel R.K., Mailloux B.J., Hall J.A., Onstott T.C., Fredickson J.C., Balkwill D.L., DeFlaun M.F. Development of a vital fluorescent staining method for monitoring bacterial transport in subsurface environments. Appl. Environ. Microbiol. 2000, 66:4486-4496.
23. Gagliostro G.A. Nutritional control of conjugated linoleic acid (CLA) content in milk and in natural food. Rev. Arg. Prod. Anim. 2005, 24:137-163.
24. Gorissen L., Leroy F., De Vuyst L., De Smet S., Raes K. Bacterial production of conjugated linoleic and linolenic acid in foods: A technological challenge. Crit. Rev. Food Sci. Nutr. 2015, 55:1561-1574.
25. Gorissen L., Weckx S., Vlaeminck B., Raes K., De Vuyst L., De Smet S., Leroy F. Linoleate isomerase activity occurs in lactic acid bacteria strains and is affected by pH and temperature. J. Appl. Microbiol. 2011, 111:593-606.
26. Guidone A., Zotta T., Ross R.P., Stanton C., Rea M.C., Parente E., Ricciardi A. Functional properties of Lactobacillus plantarum strains: A multivariate screening study. LWT-. Food Sci. Technol. (Campinas.) 2014, 56:69-76.
27. Herman-Lara E., Santos-Blanco V.M., Vivar-Vera M.A., García H.S., Ochoa-Martínez L.A., Martínez-Sánchez C.E. Conjugated linoleic acid content in selected Mexican beef and dairy products. CyTA-J. Food 2012, 10:71-77.
28. Hernández-Mendoza A., Lopez-Hernandez A., Hill C.G., Garcia H.S. Bioconversion of linoleic acid to conjugated linoleic acid by Lactobacillus reuteri under different growth conditions. J. Chem. Technol. Biotechnol. 2009, 84:180-185.
29. Huang Y., Adams M.C. In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy Propionibacteria. Int. J. Food Microbiol. 2004, 91:253-260.
30. Ip C., Lisk D.J., Scimeca J.A. Potential of food modification in cancer prevention. Cancer Res. 1994, 54:1957s-1959s.
31. Kabak B., Ozbey F. Aflatoxin M1 in UHT milk consumed in Turkey and first assessment of its bioaccessibility using an in vitro digestion model. Food Contr. 2012, 28:338-344.
32. Kajfasz J.K., Quivey R.J. Responses of lactic acid bacteria to acid stress. Stress Responses of Lactic Acid Bacteria 2011, 23-53. Springer, New York, NY. E. Tsakalidou, K. Papadimitriou (Eds.).
33. Kaushik J.K., Kumar A., Duary R.K., Mohanty A.K., Grover S., Batish V.K. Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PLoS ONE 2009, 4:e8099. http://dx.doi.org/10.1371/journal.pone.0008099.
34. Kim Y.J., Liu R.H. Increase of conjugated linoleic acid content in milk by fermentation with lactic acid bacteria. J. Food Sci. 2002, 67:1731-1737.
35. Kos B., Suskovic J., Goreta J., Matosic S. Effect of protectors on the viability of Lactobacillus acidophilus M92 in simulated gastrointestinal conditions. Food Technol. Biotechnol. 2000, 38:121-127.
36. Lee H.Y., Park J.H., Seok S.H., Baek M.W., Kim D.J., Lee K.E., Paek K.S., Lee Y. Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim. Biophys. Acta 2006, 1761:736-744.
37. Lee K., Lee Y. Production of c9,t11- and t10,c12-conjugated linoleic acids in humans by Lactobacillus rhamnosus PL60. J. Microbiol. Biotechnol. 2009, 19:1617-1619.
38. Lee K., Paek K., Lee H.Y., Park J.H., Lee Y. Antiobesity effect of trans-10,cis-12-conjugated linoleic acid-producing Lactobacillus plantarum PL62 on diet-induced obese mice. J. Appl. Microbiol. 2007, 103:1140-1146.
39. Lee Y.K., Ho P.S., Low C.S., Arvilommi H., Salminen S. Permanent colonization by Lactobacillus casei is hindered by the low rate of cell division in mouse gut. Appl. Environ. Microbiol. 2004, 70:670-674.
40. Lima Alves L., Santos Richards N., Mariutti L., Nogueira G., Bragagnolo N. Inulin and probiotic concentration effects on fatty and linoleic conjugated acids in cream cheeses. Eur. Food Res. Technol. 2011, 233:667-675.
41. Lin H., Boylston T.D., Chang M.J., Luedecke L.O., Shultz T.D. Survery of the conjugated linoleic acid contents of dairy products. J. Dairy Sci. 1995, 78:2358-2365.
42. Liu P., Shen S.R., Ruan H., Zhou Q., Ma L.L., He G.Q. Production of conjugated linoleic acids by Lactobacillus plantarum strains isolated from naturally fermented Chinese pickles. J. Zhejiang Univ. Sci. B 2011, 12:923-930.
43. Moser S.A., Savage D.C. Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in Lactobacilli. Appl. Environ. Microbiol. 2001, 67:3476-3480.
44. Nunes J.C., Torres A.G. Fatty acid and CLA composition of Brazilian dairy products, and contribution to daily intake of CLA. J. Food Compos. Anal. 2010, 23:782-789.
45. O'Shea M., Bassaganya-Riera J., Mohede I.C. Immunomodulatory properties of conjugated linoleic acid. Am. J. Clin. Nutr. 2004, 79:1199S-1206S.
46. Pandit A., Anand S., Kalscheur K., Hassan A. Production of conjugated linoleic acid by lactic acid bacteria in milk without any additional substrate. Int. J. Dairy Technol. 2012, 65:603-608.
47. Parish C.R. Fluorescent dyes for lymphocyte migration and proliferation studies. Immunol. Cell Biol. 1999, 77:499-508.
48. Park Y. Conjugated linoleic acid (CLA): Good or bad trans fat?. J. Food Compos. Anal. 2009, 22:4-12.
49. Prandini A., Sigolo S., Tansini G., Brogna N., Piva G. Different level of conjugated linoleic acid (CLA) in dairy products from Italy. J. Food Compos. Anal. 2007, 20:472-479.
50. Puniya A., Reddy C., Kumar S., Singh K. Influence of sunflower oil on conjugated linoleic acid production by Lactobacillus acidophilus and Lactobacillus casei. Ann. Microbiol. 2009, 59:505-507.
51. Rett B.S., Whelan J. Increasing dietary linoleic acid does not increase tissue arachidonic acid content in adults consuming Western-type diets: A systematic review. Nutr. Metab. (Lond.) 2011, 8:36.
52. Rodríguez-Alcala L.M., Braga T., Xavier Malcata F., Gomes A., Fontecha J. Quantitative and qualitative determination of CLA produced by Bifidobacterium and lactic acid bacteria by combining spectrophotometric and Ag+-HPLC techniques. Food Chem. 2011, 125:1373-1378.
53. Roman-Nunez M., Cuesta-Alonso E.P., Gilliland S.E. Influence of sodium glycocholate on production of conjugated linoleic acid by cells of Lactobacillus reuteri ATCC 55739. J. Food Sci. 2007, 72:M140-143.
54. Taranto M.P., Perez-Martinez G., Font de Valdez G. Effect of bile acid on the cell membrane functionality of lactic acid bacteria for oral administration. Res. Microbiol. 2006, 157:720-725.
55. Van Nieuwenhove C.P., Oliszewski R., Gonzalez S.N., Perez Chaia A.B. Conjugated linoleic acid conversion by dairy bacteria cultured in MRS broth and buffalo milk. Lett. Appl. Microbiol. 2007, 44:467-474. a.
56. Van Nieuwenhove C.P., Oliszewski R., González S.N., Pérez Chaia A.B. Influence of bacteria used as adjunct culture and sunflower oil addition on conjugated linoleic acid content in buffalo cheese. Food Res. Int. 2007, 40:559-564. b.
57. Wall R., Ross R.P., Shanahan F., O'Mahony L., O'Mahony C., Coakley M., Hart O., Lawlor P., Quigley E.M., Kiely B., Fitzgerald G.F., Stanton C. Metabolic activity of the enteric microbiota influences the fatty acid composition of murine and porcine liver and adipose tissues. Am. J. Clin. Nutr. 2009, 89:1393-1401.
58. Wang X.Q., Duan X.M., Liu L.H., Fang Y.Q., Tan Y. Carboxyfluorescein diacetate succinimidyl ester fluorescent dye for cell labeling. Acta Biochim. Biophys. Sin. (Shanghai) 2005, 37:379-385.
59. Whigham L.D., Watras A.C., Schoeller D.A. Efficacy of conjugated linoleic acid for reducing fat mass: A meta-analysis in humans. Am. J. Clin. Nutr. 2007, 85:1203-1211.
60. Xu S., Boylston T., Glatz B. Effect of lipid source on probiotic bacteria and conjugated linoleic acid formation in milk model systems. J. Am. Oil Chem. Soc. 2004, 81:589-595.