Skip to main content
Log in

Characterization of Probiotic Properties of Antifungal Lactobacillus Strains Isolated from Traditional Fermenting Green Olives

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

Abstract

The aim of this work is to characterize the potential probiotic properties of 14 antifungal Lactobacillus strains isolated from traditional fermenting Moroccan green olives. The molecular identification of strains indicated that they are composed of five Lactobacillus brevis, two Lactobacillus pentosus, and seven Lactobacillus plantarum. In combination with bile (0.3%), all the strains showed survival rates (SRs) of 83.19–56.51% at pH 3, while 10 strains showed SRs of 31.67–64.44% at pH 2.5. All the strains demonstrated high tolerance to phenol (0.6%) and produced exopolysaccharides. The autoaggregation, hydrophobicity, antioxidant activities, and surface tension value ranges of the strains were 10.29–41.34%, 15.07–34.67%, 43.11–52.99%, and 36.23–40.27 mN/m, respectively. Bacterial cultures exhibited high antifungal activity against Penicillium sp. The cell-free supernatant (CFS) of the cultures showed important inhibition zones against Candida pelliculosa (18.2–24.85 mm), as well as an antibacterial effect against some gram-positive and gram-negative bacteria (10.1–14.1 mm). The neutralized cell-free supernatant of the cultures displayed considerable inhibitory activity against C. pelliculosa (11.2–16.4 mm). None of the strains showed acquired or horizontally transferable antibiotic resistance or mucin degradation or DNase, hemolytic, or gelatinase activities. Lactobacillus brevis S82, Lactobacillus pentosus S75, and Lactobacillus plantarum S62 showed aminopeptidase, β-galactosidase, and β-glucosidase activities, while the other enzymes of API-ZYM were not detected. The results obtained revealed that the selected antifungal Lactobacillus strains are considered suitable candidates for use both as probiotic cultures for human consumption and for starters and as biopreservative cultures in agriculture, food, and pharmaceutical industries.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food London, Ontario, Canada, April 30 and May 1, (2002) http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf. Accessed 10 May 2018

  2. Speranza B, Racioppo A, Beneduce L, Bevilacqua A, Sinigaglia M, Corbo MR (2017) Autochthonous lactic acid bacteria with probiotic aptitudes as starter cultures for fish-based products. Food Microbiol 65:244–253. https://doi.org/10.1016/j.fm.2017.03.010

    Article  CAS  PubMed  Google Scholar 

  3. Mizock BA (2015) Probiotics. Dis Mon 61(7):259–290. https://doi.org/10.1016/j.disamonth.2015.03.011

    Article  PubMed  Google Scholar 

  4. Saarela M, Mogensen G, Fonden R, Matto J, Mattila-Sandholm T (2000) Probiotic bacteria: safety, functional and technological properties. J Biotechnol 84(3):197–215. https://doi.org/10.1016/S0168-1656(00)00375-8

    Article  CAS  PubMed  Google Scholar 

  5. Ammor MS, Mayo B (2007) Selection criteria for lactic acid bacteria to be used as functional starter cultures in dry sausage production: an update. Meat Sci 76(1):138–146. https://doi.org/10.1016/j.meatsci.2006.10.022

    Article  CAS  PubMed  Google Scholar 

  6. Aswathy RG, Ismail B, John RP, Nampoothiri KM (2008) Evaluation of the probiotic characteristics of newly isolated lactic acid bacteria. Appl Biochem Biotechnol 151(2–3):244–255. https://doi.org/10.1007/s12010-008-8183-6

    Article  CAS  PubMed  Google Scholar 

  7. Tambekar DH, Bhutada SA (2010) An evaluation of probiotic potential of Lactobacillus sp. from milk of domestic animals and commercial available probiotic preparations in prevention of enteric bacterial infections. Recent Res Sci Technol 2(10):82–88

    Google Scholar 

  8. Kumar A, Kumar D (2015) Characterization of Lactobacillus isolated from dairy samples for probiotic properties. Anaerobe 33:117–123. https://doi.org/10.1016/j.anaerobe.2015.03.004

    Article  CAS  PubMed  Google Scholar 

  9. Ren D, Li C, Qin Y, Yin R, Du S, Ye F, Liu C, Liu H, Wang M, Li Y, Sun Y, Li X, Tian M, Jin N (2014) In vitro evaluation of the probiotic and functional potential of Lactobacillus strains isolated from fermented food and human intestine. Anaerobe 30:1–10. https://doi.org/10.1016/j.anaerobe.2014.07.004

    Article  CAS  PubMed  Google Scholar 

  10. Pringsulaka O, Rueangyotchanthana K, Suwannasai N, Watanapokasin R, Amnueysit P, Sunthornthummas S, Sukkhum S, Sarawaneeyaruk S, Rangsiruji A (2015) In vitro screening of lactic acid bacteria for multi-strain probiotics. Livest Sci 174:66–73. https://doi.org/10.1016/j.livsci.2015.01.016

    Article  Google Scholar 

  11. Cao Z, Pan H, Tong H, Gu D, Li S, Xu Y, Ge C, Lin Q (2015) In vitro evaluation of probiotic potential of Pediococcus pentosaceus L1 isolated from paocai—a Chinese fermented vegetable. Ann Microbiol 66(3):963–971. https://doi.org/10.1007/s13213-015-1182-2

    Article  CAS  Google Scholar 

  12. Jampaphaeng K, Cocolin L, Maneerat S (2016) Selection and evaluation of functional characteristics of autochthonous lactic acid bacteria isolated from traditional fermented stinky bean (Sataw-Dong). Ann Microbiol 67(1):25–36. https://doi.org/10.1007/s13213-016-1233-3

    Article  CAS  Google Scholar 

  13. Khan I, Kang SC (2016) Probiotic potential of nutritionally improved Lactobacillus plantarum DGK-17 isolated from kimchi—a traditional Korean fermented food. Food Control 60:88–94. https://doi.org/10.1016/j.foodcont.2015.07.010

    Article  CAS  Google Scholar 

  14. Makete G, Aiyegoro OA, Thantsha MS (2017) Isolation, identification and screening of potential probiotic bacteria in milk from south African saanen goats. Probiotics Antimicrob Proteins 9(3):246–254. https://doi.org/10.1007/s12602-016-9247-5

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  CAS  Google Scholar 

  16. Motahari P, Mirdamadi S, Kianirad M (2017) Safety evaluation and antimicrobial properties of Lactobacillus pentosus 22C isolated from traditional yogurt. J Food Meas Charact 11(3):972–978. https://doi.org/10.1007/s11694-017-9471-z

    Article  Google Scholar 

  17. Aarti C, Khusro A, Varghese R, Arasu MV, Agastian P, Al-Dhabi NA, Ilavenil S, Choi KC (2017) In vitro studies on probiotic and antioxidant properties of Lactobacillus brevis strain LAP2 isolated from hentak, a fermented fish product of north-east India. LWT-Food Sci Technol 86:438–446. https://doi.org/10.1016/j.lwt.2017.07.055

    Article  CAS  Google Scholar 

  18. Aarti C, Khusro A, Varghese R, Arasu MV, Agastian P, Al-Dhabi NA, Ilavenil S, Choi KC (2018) In vitro investigation on probiotic, anti-Candida, and antibiofilm properties of Lactobacillus pentosus strain LAP1. Arch Oral Biol 89:99–106. https://doi.org/10.1016/j.archoralbio.2018.02.014

    Article  CAS  PubMed  Google Scholar 

  19. Rokni Y, Ghabbour N, Chihib NE, Thonart P, Asehraou A (2015) Physico-chemical and microbiological characterization of the natural fermentation of Moroccan picholine green olives variety. J Mater Environ Sci 6(6):1740–1751

    CAS  Google Scholar 

  20. Peres CM, Alves M, Hernandez-Mendoza A, Moreira L, Silva S, Bronze MR, Vilas-Boas L, Peres C, Malcata FX (2014) Novel isolates of lactobacilli from fermented Portuguese olive as potential probiotics. LWT-Food Sci Technol 59(1):234–246. https://doi.org/10.1016/j.lwt.2014.03.003

    Article  CAS  Google Scholar 

  21. Argyri AA, Zoumpopoulou G, Karatzas KA, Tsakalidou E, Nychas GJ, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33(2):282–291. https://doi.org/10.1016/j.fm.2012.10.005

    Article  CAS  PubMed  Google Scholar 

  22. Bevilacqua A, Altieri C, Corbo MR, Sinigaglia M, Ouoba LI (2010) Characterization of lactic acid bacteria isolated from Italian Bella di Cerignola table olives: selection of potential multifunctional starter cultures. J Food Sci 75(8):M536–M544. https://doi.org/10.1111/j.1750-3841.2010.01793.x

    Article  CAS  PubMed  Google Scholar 

  23. Bautista-Gallego J, Arroyo-López FN, Rantsiou K, Jiménez-Díaz R, Garrido-Fernández A, Cocolin L (2013) Screening of lactic acid bacteria isolated from fermented table olives with probiotic potential. Food Res Int 50(1):135–142. https://doi.org/10.1016/j.foodres.2012.10.004

    Article  CAS  Google Scholar 

  24. Ghabbour N, Lamzira Z, Thonart P, Cidalia P, Markaoui M, Asehraou A (2011) Selection of oleuropein-degrading lactic acid bacteria strains isolated from fermenting Moroccan green olives. Grasas Aceites 62(1):84–89. https://doi.org/10.3989/gya.055510

    Article  CAS  Google Scholar 

  25. Ghabbour N, Rokni Y, Lamzira Z, Thonart P, Chihib NE, Peres C, Asehraou A (2016) Controlled fermentation of Moroccan picholine green olives by oleuropein-degrading lactobacilli strains. Grasas Aceites 67(2):e138. https://doi.org/10.3989/gya.0759152

    Article  CAS  Google Scholar 

  26. Henning C, Vijayakumar P, Adhikari R, Jagannathan B, Gautam D, Muriana PM (2015) Isolation and taxonomic identity of bacteriocin-producing lactic acid bacteria from retail foods and animal sources. Microorganisms 3(1):80–93. https://doi.org/10.3390/microorganisms3010080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rokni Y (2017) Contribution à l’étude de la biodégradation de l’oleuropéine par des souches de bactéries lactiques et de levures isolées des olives vertes en fermentation naturelle. Doctorat en Sciences, Université Mohammed Premier, Maroc

  28. Bergey DH (2009) Bergey’s manual of systematic bacteriology. Springer-Verlag, New York

    Google Scholar 

  29. Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Niu C, Yang Z, Wang Q (2012) Antioxidant activity of Lactobacillus plantarum strains 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 

  30. Angmo K, Kumari A, Savitri, Bhalla TC (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

    Article  CAS  Google Scholar 

  31. Magnusson J, Schnurer J (2001) Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Appl Environ Microbiol 67(1):1–5. https://doi.org/10.1128/AEM.67.1.1-5.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ram Kumar P, Rana S, Kashyap N, Kaur A (2013) Probiotic potential of lactic acid bacteria isolated from food samples: an in vitro study. J Appl Pharm Sci 3(3):85–93. https://doi.org/10.7324/japs.2013.30317

    Article  Google Scholar 

  33. Zhou JS, Gopal PK, Gill HS (2001) Potential probiotic lactic acid bacteria Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019) do not degrade gastric mucin in vitro. Int J Food Microbiol 63(1–2):81–90. https://doi.org/10.1016/s0168-1605(00)00398-6

    Article  CAS  PubMed  Google Scholar 

  34. Domingos-Lopes MF, Stanton C, Ross PR, Dapkevicius ML, Silva CC (2017) Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal pico cheese. Food Microbiol 63:178–190. https://doi.org/10.1016/j.fm.2016.11.014

    Article  CAS  PubMed  Google Scholar 

  35. Gilliland SE, Staley TE, Bush LJ (1984) Importance of bile tolerance of Lactobacillus acidophilus used as a dietary adjunct. J Dairy Sci 67(12):3045–3051. https://doi.org/10.3168/jds.S0022-0302(84)81670-7

    Article  CAS  PubMed  Google Scholar 

  36. Gu RX, Yang ZQ, Li ZH, Chen SL, Luo ZL (2008) Probiotic properties of lactic acid bacteria isolated from stool samples of longevous people in regions of Hotan, Xinjiang and Bama, Guangxi, China. Anaerobe 14(6):313–317. https://doi.org/10.1016/j.anaerobe.2008.06.001

    Article  CAS  PubMed  Google Scholar 

  37. 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 

  38. Lee KW, Shim JM, Park S-K, Heo H-J, Kim H-J, Ham K-S, Kim JH (2016) Isolation of lactic acid bacteria with probiotic potentials from kimchi, traditional Korean fermented vegetable. LWT-Food Sci Technol 71:130–137. https://doi.org/10.1016/j.lwt.2016.03.029

    Article  CAS  Google Scholar 

  39. Bonatsou S, Tassou CC, Panagou EZ, Nychas GE (2017) Table olive fermentation using starter cultures with multifunctional potential. Microorganisms 5(2):30. https://doi.org/10.3390/microorganisms5020030

    Article  CAS  PubMed Central  Google Scholar 

  40. Casarotti SN, Carneiro BM, Todorov SD, Nero LA, Rahal P, Penna ALB (2017) In vitro assessment of safety and probiotic potential characteristics of Lactobacillus strains isolated from water buffalo mozzarella cheese. Ann Microbiol 67(4):289–301. https://doi.org/10.1007/s13213-017-1258-2

    Article  CAS  Google Scholar 

  41. Anandharaj M, Sivasankari B, Santhanakaruppu R, Manimaran M, Rani RP, Sivakumar S (2015) Determining the probiotic potential of cholesterol-reducing Lactobacillus and Weissella strains isolated from gherkins (fermented cucumber) and south Indian fermented koozh. Res Microbiol 166(5):428–439. https://doi.org/10.1016/j.resmic.2015.03.002

    Article  CAS  PubMed  Google Scholar 

  42. Kaushik JK, Kumar A, Duary RK, Mohanty AK, Grover S, Batish VK (2009) Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PLoS One 4(12):e8099. https://doi.org/10.1371/journal.pone.0008099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ji K, Jang NY, Kim YT (2015) Isolation of lactic acid bacteria showing antioxidative and probiotic activities from kimchi and infant feces. J Microbiol Biotechnol 25(9):1568–1577. https://doi.org/10.4014/jmb.1501.01077

    Article  CAS  PubMed  Google Scholar 

  44. Azat R, Liu Y, Li W, Kayir A, Lin DB, Zhou WW, Zheng XD (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 

  45. Son S-H, Jeon H-L, Jeon EB, Lee N-K, Park Y-S, Kang D-K, Paik H-D (2017) Potential probiotic Lactobacillus plantarum Ln4 from kimchi: evaluation of β-galactosidase and antioxidant activities. LWT-Food Sci Technol 85:181–186. https://doi.org/10.1016/j.lwt.2017.07.018

    Article  CAS  Google Scholar 

  46. Sharma D, Saharan BS (2016) Functional characterization of biomedical potential of biosurfactant produced by Lactobacillus helveticus. Biotechnol Rep 11:27–35. https://doi.org/10.1016/j.btre.2016.05.001

    Article  Google Scholar 

  47. Bakhshi N, Soleimanian-Zad S, Sheikh-Zeinoddin M (2017) Dynamic surface tension measurement for the screening of biosurfactants produced by Lactobacillus plantarum. Enzym Microb Technol 101:1–8. https://doi.org/10.1016/j.enzmictec.2017.02.010

    Article  CAS  Google Scholar 

  48. Li S, Huang R, Shah NP, Tao X, Xiong Y, Wei H (2014) Antioxidant and antibacterial activities of exopolysaccharides from Bifidobacterium bifidum WBIN03 and Lactobacillus plantarum R315. J Dairy Sci 97(12):7334–7343. https://doi.org/10.3168/jds.2014-7912

    Article  CAS  PubMed  Google Scholar 

  49. Liu Z, Zhang Z, Qiu L, Zhang F, Xu X, Wei H, Tao X (2017) Characterization and bioactivities of the exopolysaccharide from a probiotic strain of Lactobacillus plantarum WLPL04. J Dairy Sci 100(9):6895–6905. https://doi.org/10.3168/jds.2016-11944

    Article  CAS  PubMed  Google Scholar 

  50. Kanmani P, Satish Kumar R, 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 

  51. Dalié DKD, Deschamps AM, Richard-Forget F (2010) Lactic acid bacteria – potential for control of mould growth and mycotoxins: a review. Food Control 21(4):370–380. https://doi.org/10.1016/j.foodcont.2009.07.011

    Article  CAS  Google Scholar 

  52. Moreno I, Marasca ETG, de Sa P, de Souza Moitinho J, Marquezini MG, Alves MRC, Bromberg R (2018) Evaluation of probiotic potential of bacteriocinogenic lactic acid bacteria strains isolated from meat products. Probiotics Antimicrob Proteins 10(4):762–774. https://doi.org/10.1007/s12602-018-9388-9

    Article  CAS  PubMed  Google Scholar 

  53. Sharma P, Tomar SK, Sangwan V, Goswami P, Singh R (2016) Antibiotic resistance of Lactobacillus sp. isolated from commercial probiotic preparations. J Food Safety 36(1):38–51. https://doi.org/10.1111/jfs.12211

    Article  CAS  Google Scholar 

  54. Casado Munoz Mdel C, Benomar N, Lerma LL, Galvez A, Abriouel H (2014) Antibiotic resistance of Lactobacillus pentosus and Leuconostoc pseudomesenteroides isolated from naturally-fermented Aloreña table olives throughout fermentation process. Int J Food Microbiol 172:110–118. https://doi.org/10.1016/j.ijfoodmicro.2013.11.025

    Article  CAS  PubMed  Google Scholar 

  55. Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, Zhang H, Zhang W (2017) Characterization of antibiotic resistance genes from Lactobacillus isolated from traditional dairy products. J Food Sci 82(3):724–730. https://doi.org/10.1111/1750-3841.13645

    Article  CAS  PubMed  Google Scholar 

  56. Szatraj K, Szczepankowska AK, Chmielewska-Jeznach M (2017) Lactic acid bacteria - promising vaccine vectors: possibilities, limitations, doubts. J Appl Microbiol 123(2):325–339. https://doi.org/10.1111/jam.13446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hormannsperger G, Huys G, Levy DD, Lutgendorff F, Mack D, Phothirath P, Solano-Aguilar G, Vaughan E (2010) Safety assessment of probiotics for human use. Gut Microbes 1(3):164–185. https://doi.org/10.4161/gmic.1.3.12127

    Article  PubMed  PubMed Central  Google Scholar 

  58. Abe F, Muto M, Yaeshima T, Iwatsuki K, Aihara H, Ohashi Y, Fujisawa T (2010) Safety evaluation of probiotic bifidobacteria by analysis of mucin degradation activity and translocation ability. Anaerobe 16(2):131–136. https://doi.org/10.1016/j.anaerobe.2009.07.006

    Article  CAS  PubMed  Google Scholar 

  59. Shekh SL, Dave JM, Vyas BRM (2016) Characterization of Lactobacillus plantarum strains for functionality, safety and γ-amino butyric acid production. LWT-Food Sci Technol 74:234–241. https://doi.org/10.1016/j.lwt.2016.07.052

    Article  CAS  Google Scholar 

  60. Heavey PM, Rowland IR (2004) Microbial-gut interactions in health and disease. Gastrointestinal cancer. Best Pract Res Clin Gastroenterol 18(2):323–336. https://doi.org/10.1016/j.bpg.2003.10.003

    Article  PubMed  Google Scholar 

Download references

Funding

The authors are grateful to the CNRST (PPR/19/2015), McGill University (Quebec), CNRST-CNR (Morocco-Italy), and Tunisian cooperation (17TM06) for their support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Houssam Abouloifa.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abouloifa, H., Rokni, Y., Bellaouchi, R. et al. Characterization of Probiotic Properties of Antifungal Lactobacillus Strains Isolated from Traditional Fermenting Green Olives. Probiotics & Antimicro. Prot. 12, 683–696 (2020). https://doi.org/10.1007/s12602-019-09543-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-019-09543-8

Keywords

Navigation