Advertisement

Annals of Microbiology

, Volume 68, Issue 12, pp 803–813 | Cite as

Screening for potential probiotic from spontaneously fermented non-dairy foods based on in vitro probiotic and safety properties

  • Jing Wang
  • Jing Wang
  • Kun Yang
  • Miaomiao Liu
  • Jie Zhang
  • Xinyuan WeiEmail author
  • Mingtao FanEmail author
Original Article
  • 117 Downloads

Abstract

The aim of this study was to screen potential probiotic lactic acid bacteria from Chinese spontaneously fermented non-dairy foods by evaluating their probiotic and safety properties. All lactic acid bacteria (LAB) strains were identified by 16S rRNA gene sequencing. The in vitro probiotic tests included survival under low pH and bile salts, cell surface hydrophobicity, auto-aggregation, co-aggregation, antibacterial activity, and adherence ability to cells. The safety properties were evaluated based on hemolytic activity and antibiotic resistance profile. The salt tolerance, growth in litmus milk, and acidification ability were examined on selected potential probiotic LAB strains to investigate their potential use in food fermentation. A total of 122 strains were isolated and identified at the species level by 16S rRNA gene sequencing and included 62 Lactobacillus plantarum, 40 Weissella cibaria, 12 Lactobacillus brevis, 6 Weissella confusa, and 2 Lactobacillus sakei strains. One W. cibaria and nine L. plantarum isolates were selected based on their tolerance to low pH and bile salts. The hydrophobicity, auto-aggregation, co-aggregation, and antagonistic activities of these isolates varied greatly. All of the 10 selected strains showed multiple antibiotic resistance phenotypes and no hemolytic activity. The highest adhesion capacity to SW480 cells was observed with L. plantarum SK1. The isolates L. plantarum SK1, CB9, and CB10 were the most similar strains to Lactobacillus rhamnosus GG and selected for their high salt tolerance and acidifying activity. The results revealed strain-specific probiotic properties were and potential probiotics that can be used in the food industry.

Keywords

Lactic acid bacteria Probiotic Non-dairy food Probiotic properties 

Notes

Authors’ contributions

M.T. Fan, J. Wang, and X.Y. Wei designed the study. J. Wang, K. Yang, and M.M. Liu performed experiments and collected test data. J. Wang and J. Zhang conducted data analysis. M.T. Fan, J. Wang, and X.Y. Wei drafted the manuscript. All authors revised the manuscript.

Funding information

This work was supported by the Ministry of Agriculture of Peoples’ Republic of China (grant number 201503142-10) and the Department of Science and Technology of Shaanxi Province, China (grant number 2016NY-148; 2016KTCQ02-13).

Compliance with ethical standards

This article does not contain any studies with human participants or animals.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abushelaibi A, Al-Mahadin S, El-Tarabily K, Shah NP, Ayyash M (2017) Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT-Food Sci Technol 79:316–325.  https://doi.org/10.1016/j.lwt.2017.01.041 CrossRefGoogle Scholar
  2. Acurcio LB, Bastos RW, Sandes SHD, Guimaraes ACD, Alves CG, dos Reis DC, Wuyts S, Nunes AC, Cassali GD, Lebeer S (2017) Protective effects of milk fermented by Lactobacillus plantarum B7 from Brazilian artisanal cheese on a Salmonella enterica serovar typhimurium infection in BALB/c mice. J Funct Foods 33:436–445.  https://doi.org/10.1016/j.jff.2017.04.010 CrossRefGoogle Scholar
  3. Adimpong DB, Nielsen DS, Sørensen KI, Derkx PM, Jespersen L (2012) Genotypic characterization and safety assessment of lactic acid bacteria from indigenous African fermented food products. BMC Microbiol 12:75.  https://doi.org/10.1186/1471-2180-12-75 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ammor S, Dufour E, Zagorec M, Chaillou S, Chevallier I (2005) Characterization and selection of Lactobacillus sakei strains isolated from traditional dry sausage for their potential use as starter cultures. Food Microbiol 22:529–538.  https://doi.org/10.1016/j.fm.2004.11.016 CrossRefGoogle Scholar
  5. Angmo K, Kumari A, Savitri BTC (2016) Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. LWT-Food Sci Technol 66:428–435.  https://doi.org/10.1016/j.lwt.2015.10.057 CrossRefGoogle Scholar
  6. Argyri AA, Zoumpopoulou G, Karatizas KA, Tsakalidou E, Nychas GJ, Paganou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291.  https://doi.org/10.1016/j.fm.2012.10.005 CrossRefPubMedGoogle Scholar
  7. Atassi F, Servin AL (2010) Individual and co-operative roles of lactic acid and hydrogen peroxide in the killing activity of enteric strain Lactobacillus johnsonii NCC933 and vaginal strain Lactobacillus gasseri KS120.1 against enteric, uropathogenic and vaginosis-associated pathogens. FEMS Microbiol Lett 304:29–38.  https://doi.org/10.1111/j.1574-6968.2009.01887.x CrossRefPubMedGoogle Scholar
  8. Campana R, van Hemert S, Baffone W (2017) Strain- specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathog 9:12.  https://doi.org/10.1186/s13099-017-0162-4 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clinical and Laboratory Standards Institute (2009) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. CLSI, WayneGoogle Scholar
  10. Collado MC, Gueimonde M, Hernandez M, Sanz Y, Salminen S (2005) Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. J Food Protect 68:2672–2678.  https://doi.org/10.4315/0362-028X-68.12.2672 CrossRefGoogle Scholar
  11. Corcoran BM, Stanton C, Fitzgerald G, Ross RP (2008) Life under stress: the probiotic stress response and how it may be manipulated. Curr Pharm Design 14:1382–1399.  https://doi.org/10.2174/138161208784480225 CrossRefGoogle Scholar
  12. Danielsen M, Wind A (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1–11.  https://doi.org/10.1016/S0168-1605(02)00254-4 CrossRefPubMedGoogle Scholar
  13. Dave RI, Shah NP (1997) Viability of yogurt and probiotic bacteria in yogurts made from commercial starter cultures. Int Dairy J 7:31–41.  https://doi.org/10.1016/S0958-6946(96)00046-5 CrossRefGoogle Scholar
  14. Del Re B, Sgorbati B, Miglioli M, Palenzona D (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31:438–442.  https://doi.org/10.1046/j.1365-2672.2000.00845.x CrossRefPubMedGoogle Scholar
  15. Dicks LMT, Botes M (2010) Probiotic lactic acid bacteria in the gastro-intestinal tract: health benefits, safety and mode of action. Benef Microbes 1:11–29.  https://doi.org/10.3920/BM2009.0012 CrossRefPubMedGoogle Scholar
  16. Ding WR, Shi C, Chen M, Zhou JW, Long RJ, Guo SX (2017) Screening for lactic acid bacteria in traditional fermented Tibetan yak milk and evaluating their probiotic and cholesterol-lowering potentials in rats fed a high-cholesterol diet. J Funct Foods 32:324–332.  https://doi.org/10.1016/j.jff.2017.03.021 CrossRefGoogle Scholar
  17. Doucet-Populaire F, Trieu-Cuot P, Andremont A, Courvalin P (1992) Conjugal transfer of plasmid DNA from Enterococcus faecalis to Escherichia coli in digestive tracts of gnotobiotic mice. Antimicrob Agents Chemother 36:502–504CrossRefGoogle Scholar
  18. European Food Safety Authority (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J 10:1–10.  https://doi.org/10.2903/j.efsa.2012.2740 CrossRefGoogle Scholar
  19. FAO/WHO (2006) Probiotics in food: health and nutritional properties and guidelines for evaluation. FAO food nutrition paper 85. World Health Organization and Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  20. García-Cayuela T, Korany AM, Bustos I, Gomez de Cadiñanos LP, Requena T, Peláez C, Martínez-Cuesta M (2014) Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res Int 5:44–50.  https://doi.org/10.1016/j.foodres.2014.01.010 CrossRefGoogle Scholar
  21. Garneau-Tsodikova S, Labby KJ (2016) Mechanisms of resistance to aminoglycoside antibiotics: overview and perspectives. MedChemComm 7:11–27.  https://doi.org/10.1039/C5MD00344J CrossRefPubMedGoogle Scholar
  22. Gilliland SE, Staley TE, Bush LJ (1984) Importance in bile tolerance of Lactobacillus acidophilus used as a dietary adjunct. J Dairy Sci 67:3045–3051.  https://doi.org/10.3168/jds.S0022-0302(84)81670-7 CrossRefPubMedGoogle Scholar
  23. Goh YJ, Klaenhammer TR (2010) Functional roles of aggregation-promoting like factor in stress tolerance and adherence of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 76:5005–5015.  https://doi.org/10.1128/AEM.00030-10 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 18:716–722.  https://doi.org/10.1016/j.foodcont.2006.03.008 CrossRefGoogle Scholar
  25. Guarner F, Schaafsma GJ (1998) Probiotics. Int J Food Microbiol 39:237–238.  https://doi.org/10.1016/S0168-1605(97)00136-0 CrossRefPubMedGoogle Scholar
  26. Guo Z, Wang J, Yan L, Chen W, Liu X, Zhang H (2009) In vitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains. LWT–Food Sci Technol 42:1640–1646.  https://doi.org/10.1016/j.lwt.2009.05.025 CrossRefGoogle Scholar
  27. Guo L, Li T, Tang Y, Yang L, Huo G (2016) Probiotic properties of Enterococcus strains isolated from traditional naturally fermented cream in China. Microb Biotechnol 9:737–745.  https://doi.org/10.1111/1751-7915.12306 CrossRefPubMedGoogle Scholar
  28. Han Q, Kong BH, Chen Q, Sun FD, 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 CrossRefGoogle Scholar
  29. Hyacinta M, Hana KS, Andrea B, Barbora C (2015) Bile tolerance and its effect on antibiotic susceptibility of probiotic Lactobacillus candidates. Folia Microbiol 60:253–257.  https://doi.org/10.1007/s12223-014-0365-8 CrossRefGoogle Scholar
  30. Jacobsen L, Wilcks A, Hammer K, Huys G, Gevers D, Andersen SR (2007) Horizontal transfer of tet(M) and erm(B) resistance plasmids from food strains of Lactobacillus plantarum to Enterococcus faecalis JH2–2 in the gastrointestinal tract of gnotobiotic rats. FEMS Microbiol Ecol 59:158–166.  https://doi.org/10.1111/j.1574-6941.2006.00212.x CrossRefPubMedGoogle Scholar
  31. Jampaphaeng K, Cocolin L, Maneerat S (2017) Selection and evaluation of functional characteristics of autochthonous lactic acid bacteria isolated from traditional fermented stinky bean (Sataw-Dong). Ann Microbiol 67:25–36.  https://doi.org/10.1007/s13213-016-1233-3 CrossRefGoogle Scholar
  32. Klingberg TD, Axelsson L, Naterstad K, Elsser D, Budde BB (2005) Identification of potential probiotic starter cultures for Scandinavian-type fermented sausages. Int J Food Microbiol 105:419–431.  https://doi.org/10.1016/j.ijfoodmicro.2005.03.020 CrossRefPubMedGoogle Scholar
  33. Kos B, Šušković J, Vuković S, Šimpraga M, Frece J, Matošić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94:981–987.  https://doi.org/10.1046/j.1365-2672.2003.01915.x CrossRefPubMedGoogle Scholar
  34. Kotzamanidis C, Kourelis A, Litopoulou-Tzanetaki E, Tzanetakis N, Yiangou M (2010) Evaluation of adhesion capacity, cell surface traits and immunomodulatory activity of presumptive probiotic Lactobacillus strains. Int J Food Microbiol 140:154–163.  https://doi.org/10.1016/j.ijfoodmicro.2010.04.004 CrossRefPubMedGoogle Scholar
  35. Kumar BV, Vijayendra SVN, Reddy OVS (2015) Trends in dairy and non-dairy probiotic products - a review. J Food Sci Technol 52:6112–6114.  https://doi.org/10.1007/s13197-015-1795-2 CrossRefGoogle Scholar
  36. Kumar N, Tomar SK, Thakur K, Singh AK (2017) The ameliorative effects of probiotic Lactobacillus fermentum strain RS-2 on alloxan induced diabetic rats. J Funct Foods 28:275–284.  https://doi.org/10.1016/j.jff.2016.11.027 CrossRefGoogle Scholar
  37. Lee KW, Park JY, Jeong HR, Heo HJ, Han NS, Kim JH (2012) Probiotic properties of Weissella strains isolated from human faeces. Anaerobe 18:96–102.  https://doi.org/10.1016/j.anaerobe.2011.12.015 CrossRefPubMedGoogle Scholar
  38. Lee NK, Han KJ, Son SH, Eom SJ, Lee SK, Paik HD (2015) Multifunctional effect of probiotic Lactococcus lactis KC24 isolated from kimchi. LWT-Food Sci Technol 64:1036–1041.  https://doi.org/10.1016/j.lwt.2015.07.019 CrossRefGoogle Scholar
  39. Mathara JM, Schillinger U, Kutima PM, Mbugua SK, Guigas C, Franz C, Holzapfel WH (2008) Functional properties of Lactobacillus plantarum strains isolated from Maasai traditional fermented milk products in Kenya. Curr Microbiol 56:315–321.  https://doi.org/10.1007/s00284-007-9084-6 CrossRefPubMedGoogle Scholar
  40. Morandi S, 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.  https://doi.org/10.1016/j.foodcont.2011.07.011 CrossRefGoogle Scholar
  41. Moreno-Arribas V, Torlois S, Joyeux A, Bertrand A, Lonvaud-Funel A (2000) Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. J Appl Microbiol 88:584–593.  https://doi.org/10.1046/j.1365-2672.2000.00997.x CrossRefPubMedGoogle Scholar
  42. Nawaz M, Wang J, Zhou A, Ma C, Wu X, Moore JE, Millar BC, Xu J (2011) Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Curr Microbiol 62:1081–1089.  https://doi.org/10.1007/s00284-010-9856-2 CrossRefPubMedGoogle Scholar
  43. Nishida S, Michinaka A, Nakashima K, Iino H, Fujii T (2008) Evaluation of the probiotic potential of Lactobacillus paracasei KW3110 based on in vitro tests and oral administration tests in healthy adults. J Gen Appl Microbiol 54:267–276.  https://doi.org/10.2323/jgam.54.267 CrossRefPubMedGoogle Scholar
  44. Oh YJ, Dong SJ (2015) Evaluation of probiotic properties of Lactobacillus and Pediococcus strains isolated from Omegisool, a traditionally fermented millet alcoholic beverage in Korea. LWT - Food Sci Technol 63:437–444.  https://doi.org/10.1016/j.lwt.2015.03.005 CrossRefGoogle Scholar
  45. Olatunde OO, Obadina AO, Omenu AM, Oyewole OB, Olugbile A, Olukomaiya OO (2018) Screening and molecular identification of potential probiotic lactic acid bacteria in effluents generated during ogi production. Ann Microbiol 68:433–443.  https://doi.org/10.1007/s13213-018-1348-9 CrossRefGoogle Scholar
  46. Ou CC, Lu TM, Tsai JJ, Yen JH, Chen HW, Lin MY (2009) Antioxidative effect of lactic acid bacteria: intact cells vs. intracellular extracts. J Food Drug Anal 17:209–216Google Scholar
  47. Palachum W, Chisti Y, Choorit W (2018) In-vitro assessment of probiotic potential of lactobacillus plantarum WU-P19 isolated from a traditional fermented herb. Ann Microbiol 68:79–91.  https://doi.org/10.1007/s13213-017-1318-7 CrossRefGoogle Scholar
  48. Pérez Pulido R, Omar NB, Lucas R, Abriouel H, Martínez Cañamero M, Gálvez A (2005) Resistance to antimicrobial agents in lactobacilli isolated from caper fermentations. Antonie Van Leeuwenhoek 88:277–281.  https://doi.org/10.1007/s10482-005-6964-2 CrossRefPubMedGoogle Scholar
  49. Piano MD, Morellic L, Strozzib GP, Allesina S, Barbab M, Deidda F, Lorenzini P, Ballaré M, Montino F, Orsello M, Sartori M, Garello E, Carmagnola S, Pagliarulo M, Capurso L (2006) Probiotics: from research to consumer. Digest Liver Dis 38:248–255.  https://doi.org/10.1016/S1590-8658(07)60004-8 CrossRefGoogle Scholar
  50. Pieniz S, Andreazza R, Anghinoni T, Camargo F, Brandelli A (2014) Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 37:251–256.  https://doi.org/10.1016/j.foodcont.2013.09.055 CrossRefGoogle Scholar
  51. Ramasamy K, Rahman ZA, Chin SC, Alitheen NJ, Abdullah N, Wan HY (2012) Probiotic potential of lactic acid bacteria from fermented Malaysian food or milk products. Int J Food Sci Technol 47:2175–2183.  https://doi.org/10.1111/j.1365-2621.2012.03085.x CrossRefGoogle Scholar
  52. Ramos CL, Thorsen L, Schwan RF, Jespersen L (2013) Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol 36:22–29.  https://doi.org/10.1016/j.fm.2013.03.010 CrossRefPubMedGoogle Scholar
  53. Saarela M, Mogensen G, Fondén R, Mättö J, Mattila-Sandholm T (2000) Probiotic bacteria: safety, functional and technological properties. J Biotechnol 84:197–215.  https://doi.org/10.1016/S0168-1656(00)00375-8 CrossRefPubMedGoogle Scholar
  54. Saelim K, Jampaphaeng K, Maneerat S (2017) Functional properties of Lactobacillus plantarum S0/7 isolated fermented stinky bean (Sa Taw Dong) and its use as a starter culture. J Funct Foods 38:370–377.  https://doi.org/10.1016/j.jff.2017.09.035 CrossRefGoogle Scholar
  55. Succi M, Tremonte P, Reale A, Sorrentino E, Grazia L, Pacifico S, Coppola R (2005) Bile salt and acid tolerance of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. FEMS Microbiol Lett 244:129–137.  https://doi.org/10.1016/j.femsle.2005.01.037 CrossRefPubMedGoogle Scholar
  56. van Reenen CA, Dicks LM (2011) Horizontal gene transfer amongst probiotic lactic acid bacteria and other intestinal microbiota: what are the possibilities? A review. Arch Microbiol 193:157–168.  https://doi.org/10.1007/s00203-010-0668-3 CrossRefPubMedGoogle Scholar
  57. Yu J, Du X, Wang W, Zhang J, Liu W, Sun Z, Sun T, Zhang H (2011) Phenotypic and genotypic characteristics of lactic acid bacteria isolated from sour congee in Inner Mongolia of China. J Gene Appl Microbiol 57:197–206.  https://doi.org/10.2323/jgam.57.197 CrossRefGoogle Scholar
  58. Zago M, Fornasari ME, Carminati D, Burns P, Suàrez V, Vinderola G, Reinheimer J, Giraffa G (2011) Characterization and probiotic potential of Lactobacillus plantarum strains isolated from cheeses. Food Microbiol 28:1033–1040.  https://doi.org/10.1016/j.fm.2011.02.009 CrossRefPubMedGoogle Scholar
  59. Zhou N, Zhang JX, Fan MT, Wang J, Guo G, Wei XY (2012) Antibiotic resistance of lactic acid bacteria isolated from Chinese yogurts. J Dairy Sci 95:4775–4783.  https://doi.org/10.3168/jds.2011-5271 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan 2018

Authors and Affiliations

  1. 1.College of Food Science and EngineeringNorthwest A&F UniversityYanglingChina

Personalised recommendations