Probiotic Characteristics of Pediococcus pentosaceus and Apilactobacillus kunkeei Strains: The lactic Acid Bacteria Isolated from Bangladeshi Natural Honey
Applied Food Biotechnology,
Vol. 10 No. 1 (2023),
3 January 2023
,
Page 33-45
https://doi.org/10.22037/afb.v10i1.39617
Abstract
Background and Objective: Lactic acid bacteria are known for their strong probiotic effects on the hosts. The probiotic characterization of lactic acid bacteria from Bangladeshi natural honey is limited. The objectives of this study included isolation and assessment of the probiotic and safety characteristics of lactic acid bacteria in Bangladeshi honey.
Materials and Methods: Spread and streak plate techniques were used for the bacterial isolation and purification. Isolates were identified using 16S rRNA gene sequence analysis. Agar well diffusion and poisoned food methods were used for antibacterial and antifungal assessments, respectively. Antioxidant activity was carried out based on the microbial free-radical scavenging ability. Microbial autoaggregation, coaggregation and adhesion were assessed using cell sedimentation assay. Blood-agar was used in the hemolytic assay. Antibiotic susceptibility assay was carried out using disc diffusion method.
Results and Conclusion: From a total of 25 strains isolated from honey, ten Gram-positive, catalase-negative non-spore-forming isolates were selected and used in agar well diffusion assay. Three of the isolates showed prominent antimicrobial effects with large inhibition zones against all the pathogenic strains, including Bacillus cereus, Staphylococcus aureus, Vibrio cholerae, Salmonella typhi and Candida albicans. Extensive characterization of these isolates was carried out, which revealed their growth and biochemical characteristics and carbohydrate fermentation abilities. Moreover, 16S rRNA gene sequence analysis suggested that the isolates belonged to Pediococcus pentosaceus (two strains) and Apilactobacillus kunkeei. Their tolerance to simulated gastric conditions was assessed in vitro wherein the isolates showed significant survival in low pH, bile salts and phenol. They showed good adhesion ability to ethyl acetate, chloroform and xylene as well as high autoaggregation and coaggregation characteristics. Moreover, free-radical scavenging activity of the isolates suggested the presence of considerable antioxidant effects. In safety assessment, the isolates did not show hemolytic activities and were resistant to several antibiotics. Therefore, these results indicate that honey can be an important source of beneficial lactic acid bacteria species providing several probiotic advantages.
Conflict of interest: The authors declare no conflict of interest
- antimicrobial activity
- antifungal activity
- antioxidant activity
- antibiotic susceptibility
- probiotics
How to Cite
References
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https://doi.org/10.21161/mjm.180070
Hasali NH, Zamri AI, Lani MN, Mubarak A, Suhaili Z. Identification of lactic acid bacteria from Meliponine honey and their antimicrobial activity against pathogenic bacteria. Am Eurasian J Sustain Agric. 2015; 9(6):1-6.
http://eprints.unisza.edu.my/id/eprint/5044
Lashani E, Davoodabadi A, SoltanDallal MM. Some probiotic properties of Lactobacillus species isolated from honey and their antimicrobial activity against foodborne pathogens. Vet Res Forum. 2020; 11:121-126.
https://doi.org/10.30466/vrf.2018.90418.2188
Aween MM, Hassan Z, Muhialdin BJ, Noor HM, Eljamel YA. Evaluation on antibacterial activity of Lactobacillus acidophilus strains isolated from honey. Am J Appl Sci. 2012; 9: 807-817.
https://doi.org/10.3844/ajassp.2012.807.817
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https://doi.org/10.1016/j.anaerobe.2008.06.001
Akmal U, Ghori I, Elasbali AM, Alharbi B, Farid A, Alamri AS. Probiotic and antioxidant potential of the Lactobacillus spp. isolated from artisanal fermented pickles. Fermentation 2022; 8:328.
https://doi.org/10.3390/fermentation8070328
Fugaban JII, Holzapfel WH, Todorov S. The Overview of natural by-products of beneficial lactic acid bacteria as promising antimicrobial agents. Appl Food Biotechnol. 2022; 9(2): 127-143.
https://doi.org/10.22037/afb.v9i2.37544
Palachum W, Chisti Y, Choorit W. In-vitro assessment of probiotic potential of Lactobacillus plantarum WU-P19 isolated from a traditional fermented herb. Ann Microbiol. 2018; 68:79-91.
https://doi.org/10.1007/s13213-017-1318-7
Jager R, Purpura M, Farmer S, Cash HA, Keller D. Probiotic Bacillus coagulans GBI-30, 6086 improves protein absorption and utilization. Probiotics Antimicrob Proteins. 2018; 10:611-615.
https://doi.org/10.1007%2Fs12602-017-9354-y
Miller LE, Ouwehand AC, Ibarra A. Effects of probiotic-containing products on stool frequency and intestinal transit in constipated adults: Systematic review and meta-analysis of randomized controlled trials. Ann Gastroenterol. 2017; 30:629-39.
https://doi.org/10.20524/aog.2017.0192
Alard J, Peucelle V, Boutillier D, Breton J, Kuylle S, Pot B. New probiotic strains for inflammatory bowel disease management identified by combining in vitro and In vivo approaches. Benef Microbes. 2018; 9: 317-331.
https://doi.org/10.3920/BM2017.0097
Niibo M, Shirouchi B, Umegatani M, Morita Y, Ogawa A, Sakai F. Probiotic Lactobacillus gasseri SBT2055 improves insulin secretion in a diabetic rat model. J Dairy Sci. 2019; 102:997-1006.
https://doi.org/10.3168/jds.2018-15203
Mojgani N, Hussaini F, Vaseji N. Characterization of indigenous Lactobacillus strains for probiotic properties. Jundishapur J Microbiol. 2015; 8:17523.
https://doi.org/10.5812/jjm.17523
Hossain TJ, Mozumder HA, Ali F, Akther K. Inhibition of pathogenic microbes by the lactic acid bacteria Limosilactobacillus fermentum strain LAB-1 and Levilactobacillus brevis strain LAB-5 isolated from the dairy beverage borhani. Preprint. 2022.
https://doi.org/10.2139/ssrn.4056821
Alonso S, Carmen Castro M, Berdasco M, de la Banda IG, Moreno-Ventas X, de Rojas AH. Isolation and partial characterization of lactic acid bacteria from the gut microbiota of marine fishes for potential application as probiotics in aquaculture. Probiot Antimicrob Proteins. 2019; 11:569-79.
https://doi.org/10.1007/s12602-018-9439-2
Chiang SS, Pan TM. Beneficial effects of Lactobacillus paracasei subsp. paracasei NTU 101 and its fermented products. Appl Microbiol Biotechnol. 2012; 93: 903-916.
https://doi.org/10.1007/s00253-011-3753-x
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Hossain TJ, Alam M, Sikdar D. Chemical and microbiological quality assessment of raw and processed liquid market milks of Bangladesh. Cont J Food Sci Technol. 2011; 5:6-17.
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Hossain TJ, Chowdhury SI, Mozumder HA, Chowdhury MNA, Ali F, Rahman N. Hydrolytic exoenzymes produced by bacteria isolated and identified from the gastrointestinal tract of Bombay duck. Front Microbiol. 2020; 11:2097
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https://doi.org/10.1007/s10719-017-9807-2
Padmavathi T, Bhargavi R, Priyanka PR, Niranjan NR, Pavitra PV. Screening of potential probiotic lactic acid bacteria and production of amylase and its partial purification. J Genet Eng Biotechnol. 2018; 16: 357-362.
https://doi.org/10.1016/j.jgeb.2018.03.005
Zommiti M, Connil N, Hamida JB, Ferchichi M. Probiotic characteristics of Lactobacillus curvatus DN317, a strain isolated from chicken ceca. Probiotics Antimicrob Proteins. 2017: 9; 415-424.
https://doi.org/10.1007/s12602-017-9301-y
Prabhurajeshwar C, Chandrakanth RK. Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: An In vitro validation for the production of inhibitory substances. Biomed J. 2017; 40: 270-283.
https://doi.org/10.1016/j.bj.2017.06.008
Rokana N, Singh BP, Thakur N, Sharma C, Gulhane RD, Panwar H. Screening of cell surface properties of potential probiotic lactobacilli isolated from human milk. J Dairy Res. 2018; 85:347-354.
https://doi.org/10.1017/S0022029918000432
Chowdhury T, Ferdouse J. Isolation, characterization and antimicrobial activity of lactic acid bacteria from local milk and milk products. Bangladesh J Microbiol. 2016; 29(2): 76-82.
https://doi.org/10.3329/bjm.v29i2.28440
Yin J-Y, Nie S-P, Zhou C, Wan Y, Xie M-Y. Chemical characteristics and antioxidant activities of polysaccharide purified from the seeds of Plantagoasiatica L. J Sci Food Agric. 2010; 90:210-207.
https://doi.org/10.1002/jsfa.3793
Yadav R, Puniya AK, Shukla P. Probiotic properties of Lactobacillus plantarum RYPR1 from an indigenous fermented beverage Raabadi. Front Microbiol. 2016;7:1-9
https://doi.org/10.3389/fmicb.2016.01683
Moreno I, Marasca ETG, de Sa PBZR, de Souza Moitinho J, Marquezini MG, Alves MRC, Bromberg R. Evaluation of probiotic potential of bacteriocinogenic lactic acid bacteria strains isolated from meat products. Probiotics Antimicrob Proteins. 2018; 10:762-774.
https://doi.org/10.1007/s12602-018-9388-9
Ali F, Silvy TN, Hossain TJ, Uddin MK, Uddin MS. Prevalence and antimicrobial resistance phenotypes of Salmonella species recovered at various stages of broiler operations in Hathazari, Bangladesh. Int J One Health.2021; 7:158-164.
http://dx.doi.org/10.14202/IJOH.2021.158-164
Liasi SA, Azmi IT, Hassan MD, Shuhaimi M, Rosfarizan M, Ariff AB. Antimicrobial activity and antibiotic sensitivity of three isolates of lactic acid bacteria from fermented fish product, Budu. Malays J Microbiol. 2009:33-37.
https://doi.org/10.21161/mjm.15008
Uugantsetseg E, Batjargal B. Antioxidant activity of probiotic lactic acid bacteria isolated from Mongolian airag. Mong J Chem. 2014; 15:73-78.
https://doi.org/10.5564/mjc.v15i0.327
Yusuf D, Nuraida L, Dewanti-Hariyadi R, Hunaefi D. In vitro antioxidant and α-glucosidase inhibitory activities of Lactobacillus spp. isolated from Indonesian kefir grains. Appl Food Biotechnol. 2020; 8(1): 39-46.
https://doi.org/10.22037/afb.v8i1.30367
Afify AE-MM, Romeilah RM, Sultan SI, Hussein MM. Antioxidant activity and biological evaluations of probiotic bacteria strains. Int J Acad Res. 2012; 4:131-139
https://doi.org/10.7813/2075-4124.2012/4-6/A.18
Elfahri KR, Vasiljevic T, Yeager T, Donkor On. Anti-colon cancer and antioxidant activities of bovine skim milk fermented by selected Lactobacillus helveticus strains. J Dairy Sci. 2016; 99:31-40.
https://doi.org/10.3168/jds.2015-10160
AlKalbani NS, Turner MS, Ayyash MM. Isolation, identification, and potential probiotic characterization of isolated lactic acid bacteria and In vitro investigation of the cytotoxicity, antioxidant, and antidiabetic activities in fermented sausage. Microb Cell Factories. 2019; 18:1-12.
https://doi.org/10.1186/s12934-019-1239-1
Amaretti A, Di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A. Antioxidant properties of potentially probiotic bacteria: In vitro and In vivo activities. Appl Microbiol Biotechnol. 2013; 97:809-817.
https://doi.org/10.1007/s00253-012-4241-7
Sanders ME, Merenstein DJ, Reid G, Gibson GR, Rastall RA. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat Rev Gastroenterol Hepatol. 2019; 16: 605-616.
https://doi.org/10.1038/s41575-019-0173-3
Garcia EF, Luciano WA, Xavier DE, da Costa WCA, de Sousa Oliveira K, Franco OL, de Morais Junior MA, Lucena BTL, Picao RC, Magnani M, Saarela M, de Suza EL.Identification of lactic acid bacteria in fruit pulp processing byproducts and potential probiotic properties of selected Lactobacillus strains. Front Microbiol. 2016; 7.
https://doi.org/10.3389/fmicb.2016.01371
Monteagudo-Mera A, Rodriguez-Aparicio L, Rua J, Martinez-Blanco H, Navasa N, Garcia-Armesto MR, Angel Ferrero M. In vitro evaluation of physiological probiotic properties of different lactic acid bacteria strains of dairy and human origin. J Funct Foods. 2012; 4: 531-541.
https://doi.org/10.1016/j.jff.2012.02.014
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