Abstract
Objective
The objective of this study was to evaluate the probiotic potential as well as the ability of adhesion and aggregation of natural and autochthonous lactic acid bacteria, isolated from traditionally made cheese.
Results
Lactic acid bacteria from natural food sources can be promising probiotic candidates and they can be used in natural food preservation or like starter cultures. Tested autochthonous isolates showed tolerance to the simulated gastrointestinal condition as well as the sensitivity to clinically relevant antibiotics, especially to ampicillin (MIC at 0.195 μg mL−1 for lactobacilli and from 0.195 to 3.125 μg mL−1 for lactococci). Among isolates, the highest percentage of adhesion was detected with chloroform, while the adhesion ability of selected isolates to pig intestinal epithelium was in the correlation with the results of adhesion ability with solvents. The auto-aggregation ability of isolates was demonstrated, while co-aggregation with Escherichia coli was strain specific.
Conclusion
The results indicated the potential probiotic properties of the isolates and give evidence for further investigation and potential application in the dairy industry.
Similar content being viewed by others
References
Bassyouni RH, Abdel-all WS, Fadl MG, Abdel-all S, Kamel Z (2012) Characterization of lactic acid bacteria isolated from dairy products in Egypt as a probiotic. Life Sci J 9:2924–2933
Carasi P, Ambrosis NM, De Antoni GL, Bressollier P, Urdaci MC, de los Angeles Serradell M (2014) Adhesion properties of potentially probiotic Lactobacillus kefiri to gastrointestinal mucus. J Dairy Res 81(1):16–23
Collado MC, Meriluoto J, Salminen S (2008) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226:1065–1073
Dowarah R, Verma AK, Agarwal N, Singh P, Singh BR (2018) Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. PLoS ONE 13(3):e0192978. https://doi.org/10.1371/journal.pone.0192978
Elhadidy M, Zahran E (2014) Biofilm mediates Enterococcus faecalis adhesion, invasion and survival into bovine mammary epithelial cells. Lett Appl Microbiol 58:248–254
European Food Safety Authority-EFSA (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human or veterinary importance. EFSA J 10:1–10
FAO/WHO (World Health Organization) (2006) Probiotics in food. Health and nutritional properties and guidelines for evaluation. FAO Food Nutr Pap 85:2.
Garriga M, Rubio R, Aymerich T, Ruas-Madiedo P (2014) Potentially probiotic and bioprotective lactic acid bacteria starter cultures antagonise the Listeria monocytogenes adhesion to HT29 colonocyte-like cells. Benef Microbes 6(3):337–343
Hernandez-Hernandez O, Muthaiyan A, Moreno FJ, Montilla A, Sanz ML, Rickeet SC (2012) Effect of prebiotic carbohydrates on the growth and tolerance of Lactobacillus. Food Microbiol 30:355–361
Huang Y, Adams MC (2004) In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria. Int J Food Microbiol 91:253–260
Idou T (2014) Probiotic properties of Lactobacillus strains isolated from gizzard of local poultry. Iran J Microbiol 6(2):120–126
Janković T, Frece J, Abram M, Gobin I (2012) Aggregation ability of potential probiotic Lactobacillus plantarum strains. Int J Sanit Eng Res 6:19–24
Jeong DW, Lee JH (2015) Antibiotic resistance, hemolysis and biogenic amine production assessments of Leuconostoc and Weissella isolates for kimchi starter development. LWT Food Sci Technol 64:1078–1084
Kaewnopparat S, Dangmanee N, Kaewnopparat N, Srichana T, Chulasiri M, Settharaksa S (2013) In vitro probiotic properties of Lactobacillus fermentum SK5 isolated from vagina of a healthy woman. Anaerobe 22:6–13
Kaktcham PM, Zambou NF, Tchouanguep FM, El-Soda M, Choudhary MI (2012) Antimicrobial and safety properties of lactobacilli isolated from two Cameroonian traditional fermented foods. Sci Pharm 80:189–203
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
Kumar AM, Murugalatha N (2012) Isolation of Lactobacillus plantarum from cow milk and screening for the presence of sugar alcohol producing gene. J Clin Microbiol Antimicrob 4:16–22
Lee YK, Salminen S (2009) Handbook of probiotics and prebiotics. Wiley, pp 386
Leite AMO, Miguel MAL, Peixoto RS, Ruas-Madiedo P, Paschoalin VMF, Mayo B, Delgado S (2015) Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. J Dairy Sci 98:3622–3632
Li Q, Liu X, Dong M, Zhou J, Wang Y (2015) Aggregation and adhesion abilities of 18 lactic acid bacteria strains isolated from traditional fermented food. Int J Agric Policy Res 3(2):84–92
Magdoub MNI, Hassan ZMR, Effat BAM, Sadek ZIM, Tawfik NF, Mabrouk AMM (2015) Probiotic properties of some lactic acid bacteria isolated from Egyptian dairy products. Int J Curr Microbiol Appl Sci 4:758–766
Muruzović MŽ, Mladenović KG, Stefanović OD, Vasić SM, Čomić LR (2016) Extracts of Agrimonia eupatoria L. as sources of biologically active compounds and evaluation of their antioxidant, antimicrobial, and antibiofilm activities. J Food Drug Anal 24:539–547
Muruzović MŽ, Mladenović KG, Žugić Petrović TD, Čomić LR (2018a) Characterization of lactic acid bacteria isolated from traditionally made Serbian cheese and evaluation of their antagonistic potential against Enterobacteriaceae. J Food Process Preserv 42(4):e13577. https://doi.org/10.1111/jfpp.13577
Muruzović MŽ, Mladenović KG, Đilas MD, Stefanović OD, Čomić LR (2018b) In vitro evaluation of antimicrobial potential and ability of biofilm formation of autochthonous Lactobacillus spp. and Lactococcus spp. isolated from traditionally made cheese from Southeastern Serbia. J Food Process Preserv 42(11):13776
Muruzović MŽ, Mladenović KG, Čomić LR (2018) In vitro evaluation of resistance to environmental stress by planktonic and biofilm form of lactic acid bacteria isolated from traditionally made cheese from Serbia. Food Biosci 23:54–59
Ocaña V, Nader-Macías ME (2002) Vaginal lactobacilli: self- and co-aggregation ability. Br J Biomed Sci 59:183–190
Palomares IC, Morales PR, Felix AE (2007) Evaluation of probiotic properties in Lactobacillus isolated from small intestine of piglets. Rev Latinoameric Microbiol 49(3–4):46–54
Pavli PG, Argyri AA, Papadopoulou OS, Nychas GE, Chorianopoulos NG, Tassou CC (2016) Probiotic potential of lactic acid bacteria from traditional fermented dairy and meat products: assessment by in vitro tests and molecular characterization. J Probiotics Health 4:157–165
Pereira NG, Figueiredo FJB, Dias-Souza MV (2015) Antimicrobial susceptibility of commercial probiotic Lactobacillus strains. J Appl Pharm Sci 2(2):14–17
Popović N, Dinić M, Tolinački M, Mihajlović S, Terzić-Vidojević A, Bojić S, Djokić J, Golić N, Veljović K (2018) New insight into biofilm formation ability, the presence of virulence genes and probiotic potential of Enterococcus sp. dairy isolates. Front Microbiol 9:78
Pringsulaka O, Rueangyotchanthana K, Suwannasai N, Watanapokasin N, Amnueysit P, Sunthornthummas S, Sukkhum A, Sarawaneeyaruk S, Rangsiruji A (2015) In vitro screening of lactic acid bacteria for multi-strain probiotics. Livestock Sci 174:66–73
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
Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33
Sarker SD, Nahar L, Kumarasamy Y (2007) Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42:321–324
Shokryazdan P, Sieo CC, Kalavathy R, Liang JB, Alithee NB, Jahromi MF, Ho YW (2014) Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. BioMed Res Int 2014:1–16
Sitepu GR, Nursyirwani N, Efriyeldi E (2016) Adhesion of lactic acid bacteria (LAB) to intestinal epithelial cells of red snapper (Lutjanus argentimaculatus) in inhibiting Vibrio alginolyticus. J Online Mahasiswa 3(2):1–10
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 38:240–249
Šušković J, Kos B, Goreta J, Matosić S (2001) Role of lactic acid bacteria and bifidobacteria in symbiotic effect. Food Technol Biotechnol 39:227–235
Tuo Y, Yu H, Ai L, Wu Z, Guo B, Chen W (2013) Aggregation and adhesion properties of 22 Lactobacillus strains. J Dairy Sci 96:4252–4257
Uroić K, Nikolić M, Koslć B, Pavunc L, Beganović J, Lukić J, Jovčić B, Filipić B, Miljković M, Golić N, Topisirović L, Čadež N, Raspor P, Šušković J (2014) Probiotic properties of lactic acid bacteria isolated from Croatian fresh soft cheese and Serbian white pickled cheese. Food Technol Biotechnol 52:232–241
Vesković Moračanin S, Djukić D, Zdolec N, Milijašević M, Mašković P (2017) Antimicrobial resistance of lactic acid bacteria in fermented food. J Hyg Eng Des 18:25–35
Walsham ADS, MacKenzie DA, Cook V, Wemyss-Holden S, Hews CL, Juge N, Schüller S (2016) Lactobacillus reuteri inhibition of enteropathogenic Escherichia coli adherence to human intestinal epithelium. Front Microbiol 7:244
Younes JA, van der Mei HC, van den Heuvel E, Busscher HJ, Reid G (2012) Adhesion forces and coaggregation between vaginal staphylococci and lactobacilli. PLoS ONE 7(5):1–8
Živković M, Miljković MS, Ruas-Madiedo P, Markelić MB, Veljović K, Tolinački M, Sokocić S, Korać A, Golić N (2016) EPS-SJ exopolisaccharide produced by the strain Lactobacillus paracasei subsp. paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E. coli association to Caco-2 cells. Front Microbiol 7:286
Zoumpopoulou G, Foligne B, Christodoulou K, Grangette C, Pot B, Tsakalidou E (2008) Lactobacillus fermentum ACA-DC 179 displays probiotic potential in vitro and protects against trinitrobenzene sulfonic acid (TNBS)-induced colitis and Salmonella infection in murine models. Int J Food Microbiol 121:18–26
Acknowledgements
This investigation was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 41010).
Author information
Authors and Affiliations
Contributions
MŽG conceived and designed the experiments; DDN designed and photographed samples by florescent microscope and interpreted the results of adhesion; MŽG and KGM processed the results; KGM and LRČ take charge of the preparation of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflicts of interest with the current work or its publication.
Research involving human and animal participants
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Grujović, M.Ž., Mladenović, K.G., Nikodijević, D.D. et al. Autochthonous lactic acid bacteria—presentation of potential probiotics application. Biotechnol Lett 41, 1319–1331 (2019). https://doi.org/10.1007/s10529-019-02729-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-019-02729-8