Inhibiting potential of selected lactic acid bacteria isolated from Costa Rican agro-industrial waste against Salmonella sp. in yogurt

Submitted: 23 March 2024
Accepted: 9 September 2024
Published: 2 December 2024
Abstract Views: 44
PDF: 16
SUPPLEMENTARY MATERIAL: 3
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

This study aimed to characterize lactic acid bacteria (LAB) isolated from Costa Rican agro-industrial waste and explore their bioprotective potential against Salmonella in yogurt. A total of 43 LAB isolates were identified using the 16S rRNA region. In vitro inhibition of Salmonella, Listeria monocytogenes, Staphylococcus aureus, and Escherichia coli was determined. 15 of the 43 isolates showed a good to strong antimicrobial effect against at least two pathogens. 14 selected isolates were evaluated for antibiotic resistance, gelatinase, and hemolytic activity. The bioprotective effect of the most promising strain, Lactiplantibacillus pentosus, was assessed against Salmonella sp. during yogurt fermentation. All the isolates were resistant to vancomycin and showed variable degrees of susceptibility to other antibiotics. All of the isolates were negative for gelatinase, and 5 isolates had no hemolytic activity. A significant inhibitory effect of L. pentosus_58(6)-2I (p<0.05) against Salmonella during fermentation was found, but pathogen reduction was limited to 0.611 log CFU/mL.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Akpinar A, Yerlikaya O, 2021. Some potential beneficial properties of Lacticaseibacillus paracasei subsp. paracasei and Leuconostoc mesenteroides strains originating from raw milk and kefir grains. J Food Process Preserv 45:e15986. DOI: https://doi.org/10.1111/jfpp.15986
Álvarez-Cisneros YM, Ponce-Alquicira E, 2018. Antibiotic resistance in lactic acid bacteria. In: Kumar Y, ed. Antimicrobial resistance-a global threat. IntechOpen, London, UK DOI: https://doi.org/10.5772/intechopen.80624
Amenu D, Bacha K, 2024. Antagonistic effects of lactic acid bacteria isolated from Ethiopian traditional fermented foods and beverages against foodborne pathogens. Probiotics Antimicrob Proteins. doi: 10.1007/s12602-024-10231-5. DOI: https://doi.org/10.1007/s12602-024-10231-5
Amini E, Salimi F, Imanparast S, Mansour FN, 2022. Isolation and characterization of exopolysaccharide derived from Lacticaseibacillus paracasei AS20 (1) with probiotic potential and evaluation of its antibacterial activity. Lett Appl Microbiol 75:967-81. DOI: https://doi.org/10.1111/lam.13771
AOAC International, 2012. Official methods of analysis of AOAC International, 19th ed. AOAC International, Gaithersburg, MD, USA.
Asfaw T, Genetu D, Shenkute D, Shenkutie TT, Amare YE, Habteweld HA, Yitayew B, 2023. Pathogenic bacteria and their antibiotic resistance patterns in milk, yoghurt and milk contact surfaces in debre berhan town, Ethiopia. Infect Drug Resist 16:4297-309. DOI: https://doi.org/10.2147/IDR.S418793
Aziz G, Tariq M, Zaidi AH, 2021. Mining indigenous honeybee gut microbiota for Lactobacillus with probiotic potential. Microbiol 167:001032. DOI: https://doi.org/10.1099/mic.0.001032
Birnboim HC, Doly J, 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513-23. DOI: https://doi.org/10.1093/nar/7.6.1513
Carpenter DE, Ngeh-Ngwainbi J, Lee S, 1993. Lipid analysis, p. 85–104. In: Sullivan DM, Carpenter DE, eds. Methods of analysis for nutrition labeling. AOAC International, Arlington, VA, USA.
de Melo Pereira GV, de Oliveira Coelho B, Júnior AIM, Thomaz-Soccol V, Soccol CR, 2018. How to select a probiotic? A review and update of methods and criteria. Biotechnol Adv 36:2060-76. DOI: https://doi.org/10.1016/j.biotechadv.2018.09.003
Duche RT, Singh A, Wandhare AG, Sangwan V, Sihag MK, Nwagu TN, Panwar H, Ezeogu LI, 2023. Antibiotic resistance in potential probiotic lactic acid bacteria of fermented foods and human origin from Nigeria. BMC Microbiol 23:142. DOI: https://doi.org/10.1186/s12866-023-02883-0
Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC, 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843-53. DOI: https://doi.org/10.1093/nar/17.19.7843
EFSA, ECDC, 2021. The European Union one health 2019 zoonoses report. EFSA J 19:6406. DOI: https://doi.org/10.2903/j.efsa.2021.6406
El-Gazzar FE, Marth EH, 1992. Salmonellae, salmonellosis, and dairy foods: a review. J Dairy Sci 75:2327-43. DOI: https://doi.org/10.3168/jds.S0022-0302(92)77993-4
Evans MR, Salmon RL, Nehaul LM, Mably S, Wafford L, Nolan-Farrell MZ., Gardner D, Ribeiro CD, 1999. An outbreak of Salmonella Typhimurium DT170 associated with kebab meat and yoghurt relish. Epidemiol Infect 122:377-83. DOI: https://doi.org/10.1017/S0950268899002253
Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, Zang H, Zhang, W, 2017. Characterization of antibiotic resistance genes from Lactobacillus isolated from traditional dairy products. J Food Sci 82:724-30. DOI: https://doi.org/10.1111/1750-3841.13645
Hashem Y, Abdelrahman K, Aziz R, 2021. Phenotype–genotype correlations and distribution of key virulence factors in Enterococcus faecalis isolated from patients with urinary tract infections. Infect Drug 14:1713-23. DOI: https://doi.org/10.2147/IDR.S305167
Hütt P, Shchepetova J, Loivukene K, Kullisaar T, Mikelsaar M, 2006. Antagonistic activity of probiotic lactobacilli and bifidobacteria against entero- and uropathogens. J Appl Microbiol 100:1324-32. DOI: https://doi.org/10.1111/j.1365-2672.2006.02857.x
Klamm L, 2019. Klamm’s microbiology laboratory manual. Division of molecular biology and biochemistry. University of Missouri-Kansas City. Available from: https://hdl.handle.net/10355/69341.
Kumbhar SB, Ghosh JS, Samudre SP, 2009. Microbiological analysis of pathogenic organisms in indigenous fermented milk products. Adv J Food Sci Technol 1:35-8.
Liu J, Gu Z, Lu W, Hu D, Zhao X, Huang H, Zhang H, Zhao J, Chen W, 2018. Multiple mechanisms applied by Lactobacillus pentosus AT6 to mute the lethal effects of Salmonella in a mouse model. Food Funct 9:2787-95. DOI: https://doi.org/10.1039/C7FO01858D
Maasjost J, Lüschow D, Kleine A, Hafez HM, Mühldorfer K, 2019. Presence of virulence genes in Enterococcus species isolated from meat turkeys in Germany does not correlate with chicken embryo lethality. BioMed Res Int 2019:6147695. DOI: https://doi.org/10.1155/2019/6147695
Martin-Garcia A, Riu-Aumatell M, Lopez-Tamames E, 2023. Influence of process parameters on sourdough microbiota, physical properties and sensory profile. Food Rev Int 39:334-48. DOI: https://doi.org/10.1080/87559129.2021.1906698
McFrederick QS, Vuong HQ, Rothman JA, 2018. Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers. Int J Syst Evol Microbiol 68:1879-84. DOI: https://doi.org/10.1099/ijsem.0.002758
Miranda-Durán S, Porras-Reyes L, Schmidt-Durán A, 2020. Evaluation of agro-industrial residues produced in Costa Rica for a low-cost culture medium using Bacillus subtilis 168. Tecnol Marcha 33:15-25. DOI: https://doi.org/10.18845/tm.v33i4.4807
Motahari P, Mirdamadi S, Kianirad M, 2017. Safety evaluation and antimicrobial properties of Lactobacillus pentosus 22C isolated from traditional yogurt. J Food Meas Charac 11:972-8. DOI: https://doi.org/10.1007/s11694-017-9471-z
Okino Delgado CH, Fleuri LF, 2015. Orange and mango by-products: Agro-industrial waste as source of bioactive compounds and botanical versus commercial description - a review. Food Rev Int 32:1-14. DOI: https://doi.org/10.1080/87559129.2015.1041183
Olsen SJ, Ying M, Davis MF, Deasy M, Holland B, Iampietro L, Baysinger M, Sassano F, Polk L, Gormley B, Hung MJ, Pilot K, Orsini M, Van Duyne S, Rankin S, Sobel J, 2004. Multidrug-resistant Salmonella Typhimurium infection from milk contaminated after pasteurization. Emerg Infect Dis 10:932. DOI: https://doi.org/10.3201/eid1005.030484
Pan X, Chen F, Wu T, Tang H, Zhao Z, 2009. The acid, bile tolerance and antimicrobial property of Lactobacillus acidophilus NIT. Food Control 20:598-602. DOI: https://doi.org/10.1016/j.foodcont.2008.08.019
Prihanto AA, Umam NI, Bangun JD, 2024. Unveiling the secrets of Indonesian fermented fish: characteristics of lactic acid bacteria, roles, and potential in product development. Food Biosci 61:104629. DOI: https://doi.org/10.1016/j.fbio.2024.104629
Rastogi S, Mittal V, Singh A, 2021. Selection of potential probiotic bacteria from exclusively breastfed infant faeces with antagonistic activity against multidrug-resistant ESKAPE pathogens. Probiotics Antimicrob Proteins 13:739-50. DOI: https://doi.org/10.1007/s12602-020-09724-w
Santos TT, Ornellas RMS, Arcucio LB, Oliveira MM, Nicoli JR, Dias CV, Trovatti AP, Vinderola CG. 2016. Characterization of lactobacilli strains derived from cocoa fermentation in the south of Bahia for the development of probiotic cultures. LWT 73:259-66. DOI: https://doi.org/10.1016/j.lwt.2016.06.003
Savran D, Pérez F, Halkman AK, 2018a. Modeling the survival of Salmonella Enteritidis and Salmonella Typhimurium during the fermentation of yogurt. Food Sci Technol Int 24:110-6. DOI: https://doi.org/10.1177/1082013217734089
Savran D, Pérez F, Halkman AK, 2018b. Modelling survival of Salmonella Enteritidis during storage of yoghurt at different temperatures. Int J Food Microbiol 271:67-76. DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.02.017
Sharma P, Tomar SK, Sangwan V, Goswami P, Singh R, 2016. Antibiotic resistance of Lactobacillus sp. Isolated from commercial probiotic preparations. J Food Saf 36:38-51. DOI: https://doi.org/10.1111/jfs.12211
Siangpro N, Chuakrut S, Sirimanapong W, Tanasupawat S, Phongsopitanun W, Meksiriporn B, Boonnorat J, Sarin S, Kucharoenphaibul S, Jutakanoke R, 2023. Lactiplantibacillus argentoratensis and Candida tropicalis isolated from the gastrointestinal tract of fish exhibited inhibitory effects against pathogenic bacteria of Nile tilapia. Vet Sci 10:129. DOI: https://doi.org/10.3390/vetsci10020129
Singh P, Singh RV, Gupta B, Tripathi SS, Tomar KS, Jain S, Sahni YP, 2018. Prevalence study of Salmonella spp. in milk and milk products. Asian J Dairy Food Res 37:7-12. DOI: https://doi.org/10.18805/ajdfr.DR-1252
Soleimani NA, Kermanshahi RK, Yakhchali B, Sattari TN, 2010. Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. Afr J Microbiol Res 4:2169-73.
Syrokou MK, Paramithiotis S, Skandamis PN, Drosinos EH, Bosnea L, Mataragas M, 2021. High-quality draft genome sequence data of six Lactiplantibacillus plantarum subsp. argentoratensis strains isolated from various Greek wheat sourdoughs. Data Brief 37:107172. DOI: https://doi.org/10.1016/j.dib.2021.107172
Taboada NV, Alléndez G, Villalba I, López Alzogaray S, Nazareno MA, 2024. Selection of indigenous lactic acid bacteria strains to enhance the functional properties of fermented Opuntia sp. fruit juices. ACS Food Sci Technol 4:1030-8. DOI: https://doi.org/10.1021/acsfoodscitech.3c00555
Todorov SD, Weeks R, Khosravi-Darani K., Chikindas ML, 2023. Exploration and understanding of beneficial properties of lactic acid bacteria: 10 years of experience in applied food biotechnology. Appl Food Biotechnol 11:e1. DOI: https://doi.org/10.3390/microorganisms11040871
Williams EN, Van Doren JM, Leonard CL, Datta AR, 2023. Prevalence of Listeria monocytogenes, Salmonella spp., Shiga toxin-producing Escherichia coli, and Campylobacter spp. in raw milk in the United States between 2000 and 2019: a systematic review and meta-analysis. J Food Prot 86:100014. DOI: https://doi.org/10.1016/j.jfp.2022.11.006
Wu JWFW, Redondo-Solano M, Uribe L, WingChing-Jones R, Usaga J, Barboza N, 2021. First characterization of the probiotic potential of lactic acid bacteria isolated from Costa Rican pineapple silages. PeerJ 9:e12437. DOI: https://doi.org/10.7717/peerj.12437
Zhang S, Oh J, Alexander L, Ozcam M, van Pijkeren J, 2018. d-Alanyl-d-alanine ligase as a broad-host-range counterselection marker in vancomycin-resistant lactic acid bacteria. J Bacteriol 200:e00607-17. DOI: https://doi.org/10.1128/JB.00607-17

How to Cite

1.
Piedra V, Usaga J, Redondo-Solano M, Uribe-Lorío L, Valenzuela-Martínez C, Barboza N. Inhibiting potential of selected lactic acid bacteria isolated from Costa Rican agro-industrial waste against <i>Salmonella</i> sp. in yogurt. Ital J Food Safety [Internet]. 2024 Dec. 2 [cited 2024 Dec. 4];. Available from: https://www.pagepressjournals.org/ijfs/article/view/12494