Antibacterial Activity of Lactiplantibacillus Strains Isolated from Commercial Yogurt against Foodborne Pathogenic Bacteria
Applied Food Biotechnology,
Vol. 11 No. 1 (2024),
18 November 2023
,
Page e3
https://doi.org/10.22037/afb.v11i1.43275
Abstract
Abstract
Background and Objective: Lactic acid bacteria are well known as beneficial microorganisms and most of them are probiotic distributed widely, especially in fermented dairy products e.g. yogurt. This study aimed to isolate, characterize and assess antimicrobial effects of lactic acid bacteria producing bacteriocin-like inhibitory substances against foodborne pathogenic bacteria.
Material and Methods: In the present study, 17 lactic acid bacteria strains were isolated from 10 commercial yogurt samples and the antibacterial effects of lactic acid bacterial cell culture, cell-free supernatant and neutralized cell-free supernatant was assessed against standard foodborne pathogenic bacteria of Escherichia coli, Listeria monocytogenes, Klebsiella pneumonia and Salmonella typhimurium using agar well diffusion assay. Although various treatments were used, most of the lactic acid bacterial isolates showed antimicrobial activity against the foodborne pathogenic bacteria. Moreover, Lactiplantibacillus pentosus (SY1), Lacticaseibacillus rhamnosus (SY5), Lactiplantibacillus plantarum (SY8) and Lactiplantibacillus plantarum (SY9) showed significantly the best antimicrobial activity against the foodborne pathogens and thus were further identified using 16S rRNA gene molecular method.
Results and Conclusion: Results showed that four isolates could produce bacteriocin-like inhibitory substances, which was significantly effective to inhibit growth of the pathogens. Primary screening for antimicrobial activity showed that 10 lactic acid bacterial strains inhibited Escherichia coli. The results revealed that Listeria monocytogenes and Salmonella typhimurium was inhibited by six and one lactic acid bacterial isolates. Moreover, results showed that Klebsiella pneumoniae was not affected by the isolates or treatment methods. It is concluded that a bacteriocin-like inhibitory substance of lactic acid bacterial isolates was effective; hence, it could be used as a natural food additive to prevent foodborne infections and improve the food quality.
Conflict of interest: The authors declare no conflict of interest.
- Bacteriocin
- Escherichia coli
- Fermented milk
- Klebsiella pneumonia
- Lactic acid bacteria
- Salmonella typhimurium
How to Cite
References
Nyanzi R, Jooste PJ, Buys EM. Invited review: Probiotic yogurt quality criteria, regulatory framework, clinical evidence and analytical aspects. J Dairy Sci. 2021; 104: 1-19. https://doi.org/10.3168/jds.2020-19116
Sezgin E, Tekin B. Molecular evolution and population genetics of glutamate decarboxylase acid resistance pathway in lactic acid bacteria. Front Genet. 2023; 14: 1027156. https://doi.org/10.3389/fgene.2023.1027156
Jovanovic JN, Nikolic B, Seatovic S, Zavisic G, Mitic-Culafic D, Vukovic-Gacic B, Knezevic-Vukcevic J. Characterization of some potentially probiotic Lactobacillus strains of human origin. Food Sci Biotechnol. 2015;24:1781-1788. https://doi.org/10.1007/s10068-015-0232-7
Leuschner RGK, Robinson TP, Hugas M, Cocconcelli PS, Richard-Forget F, Klein G, Licht TR, Nguyen-The C, Querol A, Richardson M, Suarez JE. Qualified presumption of safety (QPS): a generic risk assessment approach for biological agents notified to the European Food Safety Authority (EFSA). Trends Food Sci Technol. 2010; 21: 425-435. https://doi.org/10.1016/j.tifs.2010.07.003
Roobab U, Batool Z, Manzoor MF, Shabbir MA, Khan MR, Aadil RM. Sources, formulations, advanced delivery and health benefits of probiotics. Curr Opin Food Sci. 2020; 32: 17-28. https://doi.org/10.1016/j.cofs.2020.01.003
Hotel A, Cordoba A. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Prevention 2001.
Fazilah NF, Ariff AB, Khayat ME, Rios-Solis L, Halim M. Influence of probiotics, prebiotics, synbiotics and bioactive phytochemicals on the formulation of functional yogurt. J Funct Foods. 2018; 48: 387-399. https://doi.org/10.1016/j.jff.2018.07.039
Riaz Rajoka MS, Shi J, Zhu J, Shao D, Huang Q, Yang H, Jin M. Capacity of lactic acid bacteria in immunity enhancement and cancer prevention. Appl Microbiol Biotechnol. 2017; 101: 35-45. https://doi.org/10.1007/s00253-016-8005-7
Mazziotta C, Tognon M, Martini F, Torreggiani E, Rotondo JC. Probiotics mechanism of action on Immune cells and beneficial effects on human health. Cells 2023; 12: 184. https://doi.org/10.3390/cells12010184
Miranda C, Contente D, Igrejas G, Camara SPA, Dapkevicius M de LE, Poeta P. Role of exposure to Lactic Acid Bacteria from foods of animal origin in human health. Foods 2021; 10: 2092. https://doi.org/10.3390/foods10092092
Prima HS, Satrianto A, Amar S. Antimicrobial potential of Limosilactobacillus fermentum isolated from Bilih fish (Mys-tacoleucus padangensis) of Singkarak Lake, west Sumatera, Indonesia. Appl Food Biotechnol. 2022; 9: 297-309. https://doi.org/10.22037/afb.v9i4.38487
Kaveh S, Hashemi SMB, Abedi E, Amiri MJ, Conte FL. Bio-preservation of meat and fermented meat products by lactic acid bacteria strains and their antibacterial metabolites. Sustainability 2023; 15: 10154. https://doi.org/10.3390/su151310154
Darbandi A, Asadi A, Mahdizade Ari M, Ohadi E, Talebi M, Halaj Zadeh M, Darb Emamie A, Ghanavati R, Kakanj M. Bacteriocins: Properties and potential use as antimicrobials. J Clin Lab Anal. 2022; 36: e24093. https://doi.org/10.1002/jcla.24093
Chen S-Y, Yang R-S, Ci B-Q, Xin W-G, Zhang Q-L, Lin L-B, Wang F. A novel bacteriocin against multiple foodborne pathogens from Lacticaseibacillus rhamnosus isolated from juice ferments: ATF perfusion-based preparation of viable cells, characterization, antibacterial and antibiofilm activity. Curr Res Food Sci. 2023; 6: 100484. https://doi.org/10.1016/j.crfs.2023.100484
Golmoradi Zadeh R, Asgharzadeh S, Darbandi A, Aliramezani A, Masjedian Jazi F. Characterization of bacteriocins produced by Lactobacillus species against adhesion and invasion of Listeria monocytogenes isolated from different samples. Microb Pathog 2022; 162: 105307. https://doi.org/10.1016/j.micpath.2021.105307
Hassan MU, Nayab H, Rehman TU, Williamson MP, Haq KU, Shafi N, Shafique F. Characterisation of bacteriocins produced by Lactobacillus spp. Isolated from the traditional Pakistani yoghurt and their antimicrobial activity against common foodborne pathogens 2020; 1-10. https://doi.org/10.1155/2020/8281623
Ismail YS, Yulvizar C, Mazhitov B. Characterization of lactic acid bacteria from local cow´s milk kefir. IOP Conf Ser Earth Environ Sci 2018; 130: 012019. https://doi.org/10.1088/1755-1315/130/1/012019
Pandian V, Thirugnanasambandan S. Isolation of bacteriocin producing lactic acid bacteria from fish gut and probiotic activity against common fresh water fish pathogen Aeromonas hydrophila. Biotechnol. 2008; 7: 124-128. https://doi.org/10.3923/biotech.2008.124.128
Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal 2016; 6: 71-79. https://doi.org/10.1016/j.jpha.2015.11.005
Udhayashree N, Senbagam D, Senthilkumar B, Nithya K, Gurusamy R. Production of bacteriocin and their application in food products. Asian Pac J Trop Biomed. 2012; 2: S406-410. https://doi.org/10.1016/S2221-1691(12)60197-X
Rzepkowska A, Zielinska D, Ołdak A, Kolożyn-Krajewska D. Safety assessment and antimicrobial properties of the lactic acid bacteria strains isolated from polish raw fermented meat products. Int J Food Prop. 2017; 20: 2736-2747. https://doi.org/10.1080/10942912.2016.1250098
Dejene F, Regasa Dadi B, Tadesse D. In vitro antagonistic effect of lactic acid bacteria isolated from fermented beverage and finfish on pathogenic and foodborne pathogenic microorganism in Ethiopia. Int J Microbiol. 2021; 2021: 1-10. https://doi.org/10.1155/2021/5370556
Azcarate-Peril MA, Raya RR. Methods for Plasmid and genomic DNA isolation from Lactobacilli. In: Spencer JFT, de Ragout Spencer AL, editors. Food Microbiol. Protoc, Totowa, NJ: Humana Press; 2001: 135-139. https://doi.org/10.1385/1-59259-029-2:135
Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB, Editors. Bergey’s Manual of Systematic Bacteriology: Volume 3: The Firmicutes. Springer Science and Business Media; 2011
Walhe RA, Diwanay SS, Patole MS, Sayyed RZ, AL-Shwaiman HA, Alkhulaifi MM, Elgorban AM, Danish S, Datta R. Cholesterol reduction and vitamin B12 production study on Enterococcus faecium and Lactobacillus pentosus Isolated from yoghurt. Sustainability 2021; 13: 5853. https://doi.org/10.3390/su13115853
Moghimi B, Ghobadi Dana M, Shapouri R, Jalili M. Antibiotic resistance profile of indigenous Streptococcus thermophilus and Lactobacillus bulgaricus strains isolated from traditional yogurt. J Food Qual. 2023; 2023: e4745784. https://doi.org/10.1155/2023/4745784
Hassan MU, Nayab H, Shafique F, Williamson MP, Alman-souri TS, Asim N, Shafi N, Attacha S, Khalid M, Ali N, Akbar N. Probiotic properties of Lactobacillus helveticus and Lactobacillus plantarum isolated from traditional pakistani yoghurt. BioMed Res Int. 2020; 2020: e8889198. https://doi.org/10.1155/2020/8889198
Martin I, Rodriguez A, Delgado J, Cordoba JJ. Strategies for Biocontrol of Listeria monocytogenes using lactic acid bacteria and their metabolites in ready-to-eat meat- and dairy-ripened products. Foods. 2022; 11: 542. https://doi.org/10.3390/foods11040542
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: 127-143. https://doi.org/10.22037/afb.v9i2.37544
Quraishi F, Fatima G, Shaheen S, Memon Z, Kainat S, Agha F. In-Vitro comparison of antimicrobial actions of probiotics (Lactobacilli species and Saccharomyces boulardii) with standard antibiotics for the treatment of diarrhea in pediatric population. Int J Clin Med. 2018; 9: 827-40. https://doi.org/10.4236/ijcm.2018.912069
Imani Fooladi AA, Chavoshi Forooshai M, Saffarian P, Mehrab R. Antimicrobial effects of four Lactobacilli strains isolated from yoghurt against Escherichia coli O157:H7. J Food Saf. 2014; 34: 150-160. https://doi.org/10.1111/jfs.12108
Yang E, Fan L, Jiang Y, Doucette C, Fillmore S. Antimicrobial activity of bacteriocin-producing lactic acid bacteria isolated from cheeses and yogurts. AMB Express. 2012; 2: 48. https://doi.org/10.1186/2191-0855-2-48
Assari F, Mojgani N, Sanjabi MR, Mirdamadi S, Jahandar H. Technological assessment of autochthonous lactic acid bacteria and their antibacterial activities against food borne pathogens in goat milk lactic cheese: LAB as bio preservative in dairy products. Appl Food Biotechnol. 2023; 10: 61-71. https://doi.org/10.22037/afb.v10i1.40001
Goa T, Beyene G, Mekonnen M, Gorems K. Isolation and characterization of lactic acid bacteria from fermented milk produced in Jimma Town, Southwest Ethiopia and evaluation of their antimicrobial activity against selected pathogenic bacteria. Int J Food Sci. 2022; 2022: e2076021. https://doi.org/10.1155/2022/2076021
Vieco-Saiz N, Belguesmia Y, Raspoet R, Auclair E, Gancel F, Kempf I, Drider D. Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front Microbiol. 2019; 10: 1-17. https://doi.org/10.3389/fmicb.2019.00057
Fadare OS, Anyadike CH, Momoh AO, Bello TK. Antimicro-bial properties, safety and probiotic attributes of lactic acid bacteria isolated from Sauerkraut. Afr J Clin Exp Microbiol. 2023; 24: 61-72.
Jose NM, Bunt CR, Hussain MA. Comparison of microbial-ogical and probiotic characteristics of Lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms 2015; 3: 198-212. https://doi.org/10.3390/microorganisms3020198
Bahri F, Lejeune A, Dubois-Dauphin R, El Mejdoub T, Boulahrouf A, Thonart P. Characterization of Lactobacillus strains isolated from algerian children faeces for their probiotic properties. Afr J Microbiol Res. 2014; 8: 297-303. https://hdl.handle.net/2268/164339
Voidarou C, Alexopoulos A, Tsinas A, Rozos G, Tzora A, Skoufos I, Varzakas T, Bezirtzoglou E. Effectiveness of bacteriocin-producing lactic acid bacteria and bifidobacterium isolated from honeycombs against spoilage microorganisms and pathogens isolated from fruits and vegetables. Appl Sci. 2020; 10: 7309. https://doi.org/10.3390/app10207309
Yazgan H, Kuley E, Guven Gokmen T, Regenstein JM, Ozogul F. The antimicrobial properties and biogenic amine production of lactic acid bacteria isolated from various fermented food products. J Food Process Preserv. 2021; 45: e15085. https://doi.org/10.1111/jfpp.15085
Sirichokchatchawan W, Pupa P, Praechansri P, Am-in N, Tanasupawat S, Sonthayanon P, Prapasarakul N. Autochtho-nous lactic acid bacteria isolated from pig faeces in Thailand show probiotic properties and antibacterial activity against enteric pathogenic bacteria. Microb Pathog. 2018; 119: 208-215.https://doi.org/10.1016/j.micpath.2018.04.031
Corsetti A, Gobbetti M, Smacchi E. Antibacterial activity of sourdough lactic acid bacteria: isolation of a bacteriocin-like inhibitory substance from Lactobacillus sanfrancisco C57. Food Microbiol. 1996; 13: 447-456. https://doi.org/10.1006/fmic.1996.0051
Heredia-Castro PY, Mendez-Romero JI, Hernandez-Mendoza A, Acedo-Felix E, Gonzalez-Cordova AF, Vallejo-Cordoba B. Antimicrobial activity and partial characterization of bacter-iocin-like inhibitory substances produced by Lactobacillus spp. isolated from artisanal Mexican cheese. J Dairy Sci 2015; 98: 8285-8293. https://doi.org/10.3168/jds.2015-10104
Wayah SB, Philip K. Pentocin MQ1: a novel, broad-spectrum, pore-forming bacteriocin from Lactobacillus pentosus CS2 With quorum sensing regulatory mechanism and biopreservative potential. Front Microbiol. 2018; 9: 564. https://doi.org/10.3389/fmicb.2018.00564
Yi L, Qi T, Hong Y, Deng L, Zeng K. Screening of bacteriocin-producing lactic acid bacteria in Chinese homemade pickle and dry-cured meat and bacteriocin identification by genome sequencing. LWT 2020; 125: 109177. https://doi.org/10.1016/j.lwt.2020.109177
Nespolo CR, Brandelli A. Production of bacteriocin-like substances by lactic acid bacteria isolated from regional ovine cheese. Braz J Microbiol 2010; 41: 1009-1018. https://doi.org/10.1590/S1517-83822010000400020
Simova ED, Beshkova DB, Dimitrov ZhP. Characterization and antimicrobial spectrum of bacteriocins produced by lactic acid bacteria isolated from traditional Bulgarian dairy products. J Appl Microbiol 2009; 106: 692-701. https://doi.org/10.1111/j.1365-2672.2008.04052.x
Fernandes P, Loureiro D, Monteiro V, Ramos C, Nero LA, Todorov SD, Guerreiro JS. Lactobacillus plantarum isolated from cheese: Production and partial characterization of bacteriocin B391. Ann Microbiol. 2017; 67: 433-442. https://doi.org/10.1007/s13213-017-1275-1
Wang Z, Zhang Y, Chen C, Fan S, Deng F, Zhao L. A novel bacteriocin isolated from Lactobacillus plantarum W3-2 and its biological characteristics. Front Nutr. 2023; 9: 1-10. https://doi.org/10.3389/fnut.2022.1111880
Man LL, Xiang DJ. Characterization of a broad spectrum bacteriocin produced by Lactobacillus plantarum MXG-68 from Inner Mongolia traditional fermented koumiss. Folia Microbiol (Praha). 2019; 64: 821-834. https://doi.org/10.1007/s12223-019-00697-0
- Abstract Viewed: 684 times
- pdf Downloaded: 798 times