Skip to main content
SpringerLink
Log in

Antioxidative and Probiotic Activities of Lactic Acid Bacteria Isolated from Traditional Artisanal Milk Cheese from Northeast China

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

The antioxidant activities and probiotic properties of lactic acid bacteria (LAB) selected from traditional artisanal milk cheese from Northeast China were investigated in this study. Among the 322 isolates, 175 LAB were identified through probiotic characterizations. Twenty-three out of the 175 strains exhibited antibacterial activity against more than four enteropathogenic bacteria. The antioxidant action of 23 LAB was evaluated by different methods, including scavenging of hydroxide radicals, DPPH radicals, superoxide anions, and ABTS+ radical cation. The ability to resist hydrogen peroxide and superoxide dismutase activity was also studied. These strains significantly showed antioxidative capacity compared with a non-antioxidative strain, closely followed by the standard probiotic strain Lactobacillus rhamnosus GG or even better. Based on 16S ribosomal RNA-sequence analysis, the 23 isolates belonged to the species Lactobacillus plantarum (16), Lactobacillus paracasei (2), Enterococcus faecium (2), Lactobacillus helveticus (1), Weissella paramesenteroides (1), and Pediococcus pentosaceus (1). In addition, five out of the 23 strains were susceptible to most of the tested antibiotics, showed extremely high levels of hydrophobicity similar to or better than the reference strain L. rhamnosus GG, and did not exhibit any hemolytic activity. These five strains were also confirmed safe through bacterial translocation. Results suggest that at least five probiotic candidates can be explored as prospective antioxidants and used as a potential antioxidant strain to be utilized in the development of functional foods and new starter cultures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72(3):215–224. https://doi.org/10.1016/S0168-1605(01)00674-2

    Article  CAS  PubMed  Google Scholar 

  2. Marx JL (1987) Oxygen free radicals linked to many diseases; the oxygen free radicals, although made as by-products of normal oxygen-using reactions, nevertheless have a wide potential for causing cell injury. Science 235:529–532

    Article  CAS  PubMed  Google Scholar 

  3. Nagmoti DM, Khatri DK, Juvekar PR, Juvekar AR (2012) Antioxidant activity free radical-scavenging potential of Pithecellobium dulce Benth seed extracts. Free Radic Antioxid 2(2):37–43. https://doi.org/10.5530/ax.2012.2.2.7

    Article  CAS  Google Scholar 

  4. Lobo V, Patil A, Phatak A, Chandra N (2010) Free radicals, antioxidants and functional foods: impact on human health. Pharmacogn Rev 4(8):118–126. https://doi.org/10.4103/0973-7847.70902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Simic MG (1988) Mechanisms of inhibition of free-radical processes in mutagenesis and carcinogenesis. Mutat Res 202(2):377–386. https://doi.org/10.1016/0027-5107(88)90199-6

    Article  CAS  PubMed  Google Scholar 

  6. Luo D, Fang B (2008) Structural identification of ginseng polysaccharides and testing of their antioxidant activities. Carbohydr Polym 72(3):376–381. https://doi.org/10.1016/j.carbpol.2007.09.006

    Article  CAS  Google Scholar 

  7. Czerwińska M, Kiss AK, Naruszewicz M (2012) A comparison of antioxidant activities of oleuropein and its dialdehydic derivative from olive oil, oleacein. Food Chem 131(3):940–947. https://doi.org/10.1016/j.foodchem.2011.09.082

    Article  CAS  Google Scholar 

  8. Ayeni FA, Sánchez B, Adeniyi BA, Clara G, Margolles A, Ruas-Madiedo P (2011) Evaluation of the functional potential of Weissella and Lactobacillus isolates obtained from Nigerian traditional fermented foods and cow’s intestine. Int J Food Microbiol 147(2):97–104. https://doi.org/10.1016/j.ijfoodmicro.2011.03.014

    Article  PubMed  Google Scholar 

  9. Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15(2):67–78. https://doi.org/10.1016/j.tifs.2003.09.004

    Article  CAS  Google Scholar 

  10. Holzapfel WH, Schillinger U (2002) Introduction to pre-and probiotics. Food Res Int 35(2–3):109–116. https://doi.org/10.1016/S0963-9969(01)00171-5

    Article  Google Scholar 

  11. Hashemi SMB, Shahidi F, Mortazavi SA, Milani E, Eshaghi Z (2014) Potentially probiotic Lactobacillus strains from traditional Kurdish cheese. Probiotics Antimicrob Proteins 6(1):22–31. https://doi.org/10.1007/s12602-014-9155-5

    Article  CAS  PubMed  Google Scholar 

  12. Kaizu H, Sasaki M, Nakajima H, Suzuki Y (1993) Effect of antioxidative lactic acid bacteria on rats fed a diet deficient in vitamin E. J Dairy Sci 76(9):2493–2499. https://doi.org/10.3168/jds.S0022-0302(93)77584-0

    Article  CAS  PubMed  Google Scholar 

  13. Kullisaar T, Songisepp E, Mikelsaar M, Zilmer K, Vihalemm T, Zilmer M (2003) Antioxidative probiotic fermented goats’ milk decreases oxidative stress-mediated atherogenicity in human subjects. Br J Nutr 90(2):449–456. https://doi.org/10.1079/BJN2003896

    Article  CAS  PubMed  Google Scholar 

  14. Nielsen B, Gürakan GC, Ünlü G (2014) Kefir: a multifaceted fermented dairy product. Probiotics Antimicrob Proteins 6(3–4):123–135. https://doi.org/10.1007/s12602-014-9168-0

    Article  CAS  PubMed  Google Scholar 

  15. Songisepp E, Kullisaar T, Hütt P, Elias P, Brilene T, Zilmer M, Mikelsaar M (2004) A new probiotic cheese with antioxidative and antimicrobial activity. J Dairy Sci 87(7):2017–2023. https://doi.org/10.3168/jds.S0022-0302(04)70019-3

    Article  CAS  PubMed  Google Scholar 

  16. Azat R, Liu Y, Li W, Kayir A, Lin D-b, Zhou W-W, Zheng X-d (2016) Probiotic properties of lactic acid bacteria isolated from traditionally fermented Xinjiang cheese. J Zhejiang Univ Sci B 17(8):597–609. https://doi.org/10.1631/jzus.B1500250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Niu C, Yang Z, Wang Q (2012) Antioxidant activity of Lactobacillus plantarum trains isolated from traditional Chinese fermented foods. Food Chem 135(3):1914–1919. https://doi.org/10.1016/j.foodchem.2012.06.048

    Article  CAS  PubMed  Google Scholar 

  18. Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei MQ (2012) Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. J Appl Microbiol 112(6):1193–1206. https://doi.org/10.1111/j.1365-2672.2012.05284.x

    Article  CAS  PubMed  Google Scholar 

  19. Pieniz S, Andreazza R, Anghinoni T, Camargo F, Brandelli A (2014) Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 37(1):251–256. https://doi.org/10.1016/j.foodcont.2013.09.055

    Article  CAS  Google Scholar 

  20. Agaliya PJ, Jeevaratnam K (2013) Molecular characterization of Lactobacilli isolated from fermented idli batter. Braz J Microbiol 44(4):1199–1206. https://doi.org/10.1590/S1517-83822013000400025

    Article  PubMed  Google Scholar 

  21. Leite AM, Miguel MA, Peixoto RS, Ruas-Madiedo P, Paschoalin VM, Mayo B, Delgado S (2015) Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. J Dairy Sci 98(6):3622–3632. https://doi.org/10.3168/jds.2014-9265

    Article  CAS  PubMed  Google Scholar 

  22. Ahire JJ, Mokashe NU, Patil HJ, Chaudhari BL (2013) Antioxidative potential of folate producing probiotic Lactobacillus helveticus CD6. J Food Sci Technol 50(1):26–34. https://doi.org/10.1007/s13197-011-0244-0

    Article  CAS  PubMed  Google Scholar 

  23. Jia N, Xiong YL, Kong B, Liu Q, Xia X (2012) Radical scavenging activity of black currant (Ribes nigrum L.) extract and its inhibitory effect on gastric cancer cell proliferation via induction of apoptosis. J Funct Foods 4(1):382–390. https://doi.org/10.1016/j.jff.2012.01.009

    Article  CAS  Google Scholar 

  24. Gao D, Gao Z, Zhu G (2013) Antioxidant effects of Lactobacillus plantarum via activation of transcription factor Nrf2. Food Funct 4(6):982–989. https://doi.org/10.1039/C3FO30316K

    Article  CAS  PubMed  Google Scholar 

  25. Solieri L, Bianchi A, Mottolese G, Lemmetti F, 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 Microbiol 38(4):240–249. https://doi.org/10.1016/j.fm.2013.10.003

    Article  CAS  PubMed  Google Scholar 

  26. Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Tech Bull Regist Med Technol 36(3):49–52. https://doi.org/10.1093/ajcp/45.4_ts.493

    Article  CAS  PubMed  Google Scholar 

  27. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16(3):189–199. https://doi.org/10.1016/j.idairyj.2005.02.009

    Article  CAS  Google Scholar 

  28. Cui X, Shi Y, Gu S, Yan X, Chen H, Ge J (2017) Antibacterial and antibiofilm activity of lactic acid bacteria isolated from traditional artisanal milk cheese from Northeast China against enteropathogenic bacteria. Probiotics Antimicrob Proteins 1:1–10. https://doi.org/10.1007/s12602-017-9364-9

    Article  CAS  Google Scholar 

  29. Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84(5):759–768. https://doi.org/10.1046/j.1365-2672.1998.00407.x

    Article  CAS  PubMed  Google Scholar 

  30. Xanthopoulos V, Litopoulou-Tzanetaki E, Tzanetakis N (2000) Characterization of Lactobacillus isolates from infant faeces as dietary adjuncts. Food Microbiol 17(2):205–215. https://doi.org/10.1006/fmic.1999.0300

    Article  Google Scholar 

  31. Usman, Hosono A (1999) Bile tolerance, taurocholate deconjugation, and binding of cholesterol by Lactobacillus gasseri strains. J Dairy Sci 82(2):243–248. https://doi.org/10.3168/jds.S0022-0302(99)75229-X

    Article  CAS  PubMed  Google Scholar 

  32. Lee NK, Yun CW, Kim SW, Chang HI, Kang CW, Paik HD (2008) Screening of Lactobacilli derived from chicken feces and partial characterization of Lactobacillus acidophilus A12 as an animal probiotics. J Microbiol Biotechnol 18(2):338–342

    CAS  PubMed  Google Scholar 

  33. Dunne C, O'Mahony L, Murphy L, Thornton G, Morrissey D, O'Halloran S, Feeney M, Flynn S, Fitzgerald G, Daly C (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73(2 Suppl):386S–392s. https://doi.org/10.1093/ajcn/73.2.386s

    Article  CAS  PubMed  Google Scholar 

  34. Turchi B, Mancini S, Fratini F, Pedonese F, Nuvoloni R, Bertelloni F, Ebani VV, Cerri D (2013) Preliminary evaluation of probiotic potential of Lactobacillus plantarum strains isolated from Italian food products. World J Microbiol Biotechnol 29(10):1913–1922. https://doi.org/10.1007/s11274-013-1356-7

    Article  PubMed  Google Scholar 

  35. Kanmani P, Satish KR, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2013) Probiotics and its functionally valuable products—a review. Crit Rev Food Sci Nutr 53(6):641–658. https://doi.org/10.1080/10408398.2011.553752

    Article  CAS  PubMed  Google Scholar 

  36. González L, Sandoval H, Sacristán N, Castro JM, Fresno JM, Tornadijo ME (2007) Identification of lactic acid bacteria isolated from Genestoso cheese throughout ripening and study of their antimicrobial activity. Food Control 18(6):716–722. https://doi.org/10.1016/j.foodcont.2006.03.008

    Article  CAS  Google Scholar 

  37. Dilna SV, Surya H, Aswathy RG, Varsha KK, Sakthikumar DN, Pandey A, Nampoothiri KM (2015) Characterization of an exopolysaccharide with potential health-benefit properties from a probiotic Lactobacillus plantarum RJF 4. LWT Food Sci Technol 64(2):1179–1186. https://doi.org/10.1016/j.lwt.2015.07.040

    Article  CAS  Google Scholar 

  38. Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57(5 Suppl):715S–725S. https://doi.org/10.1093/ajcn/57.5.715S

    Article  CAS  PubMed  Google Scholar 

  39. Wang AN, Yi XW, Yu HF, Dong B, Qiao SY (2009) Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs. J Appl Microbiol 107(4):1140–1148. https://doi.org/10.1111/j.1365-2672.2009.04294.x

    Article  CAS  PubMed  Google Scholar 

  40. Milardović S, Iveković D, Grabarić BS (2006) A novel amperometric method for antioxidant activity determination using DPPH free radical. Bioelectrochemistry 68(2):175–180. https://doi.org/10.1016/j.bioelechem.2005.06.005

    Article  CAS  PubMed  Google Scholar 

  41. Han Q, Kong B, Chen Q, Sun F, Zhang H (2017) In vitro comparison of probiotic properties of lactic acid bacteria isolated from Harbin dry sausages and selected probiotics. J Funct Foods 32:391–400. https://doi.org/10.1016/j.jff.2017.03.020

    Article  CAS  Google Scholar 

  42. De Freitas JM, Meneghini R (2001) Iron and its sensitive balance in the cell. Mutat Res 475(1–2):153–159. https://doi.org/10.1016/S0027-5107(01)00066-5

    Article  PubMed  Google Scholar 

  43. Ahotupa, Saxelin, Korpela (1996) Antioxidative properties of Lactobacillus GG. Nutr Today 31(31):51S. https://doi.org/10.1097/00017285-199611001-00018

    Article  Google Scholar 

  44. Makras L, Vuyst LD (2006) The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Int Dairy J 16(9):1049–1057. https://doi.org/10.1016/j.idairyj.2005.09.006

    Article  CAS  Google Scholar 

  45. Sanders JW, Leenhouts KJ, Haandrikman AJ, Venema G, Kok J (1995) Stress response in Lactococcus lactis: cloning, expression analysis, and mutation of the lactococcal superoxide dismutase gene. J Bacteriol 177(18):5254–5260. https://doi.org/10.1128/jb.177.18.5254-5260.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Achuthan AA, Duary RK, Madathil A, Panwar H, Kumar H, Batish VK, Grover S (2012) Antioxidative potential of lactobacilli isolated from the gut of Indian people. Mol Biol Rep 39(8):7887–7897. https://doi.org/10.1007/s11033-012-1633-9

    Article  CAS  PubMed  Google Scholar 

  47. Yang HS, Yu JC, Oh HH, Moon JS, Jung HK, Kim KJ, Choi BS, Lee JW, Chang KH (2014) Antioxidative activity of mushroom water extracts fermented by lactic acid Bacteria. J Korean Soc Food Sci Nutr 43(1):80–85. https://doi.org/10.3746/jkfn.2014.43.1.080

    Article  Google Scholar 

  48. Lee J, Hwang KT, Chung MY, Cho DH, Park CS (2010) Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect. J Food Sci 70(8):m388–m391. https://doi.org/10.1111/j.1365-2621.2005.tb11524.x

    Article  Google Scholar 

  49. García-Cayuela T, Korany AM, Bustos I, Cadiñanos LPGD, Requena T, Peláez C, Martínez-Cuesta MC (2014) Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res Int 57(1):44–50. https://doi.org/10.1016/j.foodres.2014.01.010

    Article  CAS  Google Scholar 

  50. Salyers AA, Gupta A, Wang Y (2004) Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 12(9):412–416. https://doi.org/10.1016/j.tim.2004.07.004

    Article  CAS  PubMed  Google Scholar 

  51. Ammor MS, Flórez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol 24(6):559–570. https://doi.org/10.1016/j.fm.2006.11.001

    Article  CAS  PubMed  Google Scholar 

  52. Ramiah K, Doeschate KT, Smith R, Dicks LMT (2009) Safety assessment of Lactobacillus plantarum 423 and Enterococcus mundtii ST4SA determined in trials with Wistar rats. Probiotics Antimicrob Proteins 1(1):15–23. https://doi.org/10.1007/s12602-009-9010-2

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the Chinese Natural Sciences Foundation (31672532, 31101845) and the Natural Science Foundation of Heilongjiang Province (Grant No. LC2015006).

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Northeast Agricultural University, Harbin, 150030, China

    Yunjia Shi, Xingyang Cui, Shanshan Gu, Xin Yan, Shuang Xia & Junwei Ge

  2. College of Food Science, Northeast Agricultural University, Harbin, 150030, China

    Rui Li

  3. State Key Laboratory of Veterinary Biotechnology, Heilongjiang Provincial Key Laboratory of Laboratory Animal and Comparative Medicine, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, 150069, People’s Republic of China

    Hongyan Chen

  4. Heilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Harbin, 150030, China

    Junwei Ge

Authors
  1. Yunjia Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xingyang Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shanshan Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shuang Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hongyan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junwei Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junwei Ge.

Ethics declarations

Ethical Approval/Ethics Statement

The experimental protocol (20119) was accepted by the international recommendations for animal welfare and the Ethical Committee for animal sciences of Heilongjiang Province.

Conflict of Interest

None of the authors of this paper has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, Y., Cui, X., Gu, S. et al. Antioxidative and Probiotic Activities of Lactic Acid Bacteria Isolated from Traditional Artisanal Milk Cheese from Northeast China. Probiotics & Antimicro. Prot. 11, 1086–1099 (2019). https://doi.org/10.1007/s12602-018-9452-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-018-9452-5

Keywords

Search

Navigation