Genotyping of Probiotic Lactobacilli in Nigerian Fermented Condiments for Improved Food Safety
DOI:
https://doi.org/10.3889/oamjms.2022.8338Keywords:
Fermented foods, Condiments, Genomics, Lactobacillus species, Probiotics, Starter cultureAbstract
BACKGROUND: Plant-based naturally fermented condiments usually result in poor quality products with various bacteria and fungi contaminants. Previous reports suggested the use of starter cultures from previously fermented condiments in fermentation processes to ensure health-promoting benefits, improved quality, shelf life, and organoleptic properties for the achievement of healthy nutrition, safe, and quality food.
AIM: This study aimed to genotype potential lactobacilli from locally fermented condiments for improved food safety.
METHODS: The lactobacilli colonies isolated from fermented condiments purchased from food markets in Southwest Nigeria were profiled for probiotic activities, hemolytic activities, antibiotics susceptibility, and inhibitory activities against food pathogens. Interesting probiotic lactobacilli were identified using 16S rRNA gene sequencing and evaluated for phylogenetic relatedness with other globally reported probiotic lactobacilli.
RESULTS: Lactobacillus species which expressed significant probiotics, γ-hemolysis, anti-spoilage, and anti-listerial activities (P < 0.05) with tolerable safety profiles were identified as Lactiplantibacillus plajomi YD001 (MW280136), Lactiplantibacillus plantarum YD002 (MW280139), L. plantarum YD003 (MW280137), and Lacticaseibacillus paracasei YD004 (MW280138) possessed 50.75, 50.61, 50.75, and 52.54 mol% DNA G+C contents, respectively. The species clustered into different phylogroups with high clonal relatedness with other potential lactobacilli meta-data (≥96.80%) obtained from the public repository.
CONCLUSION: Obtained genotyped Lactobacillus species are potential starter cultures for improved fermentation processes, control of food pathogens, and spoilage organisms.Downloads
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Olasupo NA, Okorie PC. African fermented food condiments: Microbiology impacts on their nutritional values. In: Frontiers and New Trends in the Science of Fermented Food and Beverages. United Kingdom: IntechOpen; 2019. https://doi.org/10.5772/intechopen.73404 DOI: https://doi.org/10.5772/intechopen.73404
Dosumu OO, Oluwaniyi OO, Awolola GV, Oyedeji OO. Nutritional composition and antimicrobial properties of three Nigerian condiments. Niger Food J. 2012;30:43-52. https://doi.org/10.1016/S0189-7241(15)30012-6 DOI: https://doi.org/10.1016/S0189-7241(15)30012-6
Afolabi FT, Abdulkadir M, Onilude AA. Isolation and screening of microorganisms Associated with Locust Bean (IRU) for the ability to ferment soya bean to produce Soy Iru. Microbiol Res J Int. 2016;13:1-10. httpss://doi.org/10.9734/BMRJ/2016/24593
Chukwu M, Ezeagwula CG, Nwakaudu AA, Oti W, Anyaogu I. Microbial loads of ogiri-ahuekere condiment produced from groundnut seed (Arachis hypogaea Linn). Agric Food Sci Res. 2019;6:114-9. http://doi.org/10.2139/ssrn.3517493 DOI: https://doi.org/10.2139/ssrn.3517493
Ezeokoli OT, Adeleke RA, Bezuidenhout CC. Core bacterial community of soy-daddawa: Insights from high-throughput DNA metabarcoding. LWT. 2018;97:61-6. https://doi.org/10.1016/j.lwt.2018.06.039 DOI: https://doi.org/10.1016/j.lwt.2018.06.039
Angadi V, Rai PK, Bara BM. Effect of organic manures and biofertilizers on plant growth, seed yield and seedling characteristics in tomato (Lycopersicon esculentum Mill.). J Pharmacogn Phytochem. 2017;6:807-10.
Çolak NG, Eken NT, Ülger M, Frary A, Doğanlar S. Mapping of quantitative trait loci for antioxidant molecules in tomato fruit: Carotenoids, Vitamins C and E, glutathione, and phenolic acids. Plant Sci. 2020;292:110393. https://doi.org/10.1016/j.plantsci.2019.110393 DOI: https://doi.org/10.1016/j.plantsci.2019.110393
Garcia-Gonzalez N, Battista N, Prete R, Corsetti A. Health-promoting role of Lactiplantibacillus plantarum isolated from fermented foods. Microorganisms. 2021;9:349. https://doi.org/10.3390/microorganisms9020349 DOI: https://doi.org/10.3390/microorganisms9020349
Olanbiwoninu AA, Odunfa SA. Microbial interaction in selected fermented vegetable condiments in Nigeria. Int Food Res J. 2018;25:439-45. http://www.ifrj.upm.edu.my
Termote C, Odongo NO, Dreyer BS, Guissou B, Parkouda C, Vinceti B. Nutrient composition of Parkia biglobosa pulp, raw and fermented seeds: A systematic review. Crit Rev Food Sci Nutr. 2020;1:1-26. https://doi.org/10.1080/10408398.2020.1813072 PMid:32914637 DOI: https://doi.org/10.1080/10408398.2020.1813072
Adewumi GA, Grover S, Isanbor C, Oguntoyinbo FA. Phylogenetics, safety and in vitro functional properties of Bacillus species isolated from Iru, a Nigerian Fermented Condiment. Korean J Microbiol Biotechnol. 2019;47:498-508. https://doi.org/10.4014/mbl.1903.03005 DOI: https://doi.org/10.4014/mbl.1903.03005
Obafemi YD, Akinduti PA, Ajayi AA, Isibor PO. Characterization and phylodiversity of implicated enteric bacteria strains in retailed tomato (Lycopersicon esculentum Mill.) fruits in southwest Nigeria. Open Access Maced J Med Sci. 2021;9:188-195. https://doi.org/10.3889/oamjms.2021.5657 DOI: https://doi.org/10.3889/oamjms.2021.5657
Uzodinma EO, Mbaeyi-Nwaoha IE, Onwurafor EU. Suitability of bacterial fermentation and foil packaging of condiment from African mesquite (Prosopis africana) seeds for nutritional retention and commercialization. Afr J Microbiol Res. 2020;14:340-8. https://doi.org/10.5897/AJMR2020.9340
Owusu-Kwarteng J, Parkouda C, Adewumi GA, Ouoba LI, Jespersen L. Technologically relevant Bacillus species and microbial safety of West African traditional alkaline fermented seed condiments. Crit Rev Food Sci Nutr. 2020;1:1-18. https://doi.org/10.1080/10408398.2020.1830026 DOI: https://doi.org/10.1080/10408398.2020.1830026
Ugwuanyi JO, Okpara AN. Current status of alkaline fermented foods and seasoning agents of Africa. In: New Advances on Fermentation Processes. United Kingdom: IntechOpen; 2019. p. 87052. https://doi.org/10.5772/intechopen.87052 DOI: https://doi.org/10.5772/intechopen.87052
Oyedepo SO, Adeyemi GA, Olawole OC, Ohijeagbon OI, Fagbemi OK, Solomon R, et al. A GIS-based method for assessment and mapping of noise pollution in Ota metropolis, Nigeria. MethodsX. 2019;6:447-57. https://doi.org/10.1016/j.mex.2019.02.027 DOI: https://doi.org/10.1016/j.mex.2019.02.027
Association of Official Analytical Chemists. Methods of Analysis International 20th Edition. Washington DC, USA: Association of Official Analytical Chemists; 2016.
Ahire JJ, Jakkamsetty C, Kashikar MS, Lakshmi SG, Madempudi RS. In vitro evaluation of probiotic properties of Lactobacillus plantarum UBLP40 isolated from traditional indigenous fermented food. Probiotics Antimicrob Proteins. 2021;13:1413-24. https://doi.org/10.1007/s12602-021-09775-7 DOI: https://doi.org/10.1007/s12602-021-09775-7
Junior WL, Guerra AF, Tarrah A, da Silva Duarte V, Giacomini A, Luchese RH, et al. Safety and stability of two potentially probiotic Lactobacillus strains after in vitro gastrointestinal transit. Probiotics Antimicrobial Proteins. 2019;1:1-10. https://doi.org/10.1007/s12602-019-09565-2 DOI: https://doi.org/10.1007/s12602-019-09565-2
Boricha AA, Shekh SL, Pithva SP, Ambalam PS, Vyas BR. In vitro evaluation of probiotic properties of Lactobacillus species of food and human origin. LWT. 2019;106:201-8. https://doi.org/10.1016/j.lwt.2019.02.021 DOI: https://doi.org/10.1016/j.lwt.2019.02.021
Atere AV, Adedeji A, Akinmoladun AC, Oyetayo VO, Akinyosoye FA. Local condiment, Iru, obtained from the fermentation of Parkia biglobosa seed substantially reduced the serum cholesterol level of wister rats. Prev Nutr Food Sci. 2020;25:153-7. https://doi.org/10.3746/pnf.2020.25.2.153 DOI: https://doi.org/10.3746/pnf.2020.25.2.153
Clinical and Laboratory Standards Institute. Methods for Antimicrobial Susceptibility Testing of Anaerobic Bacteria. 9th ed., Vol. 9. United States of America: Clinical and Laboratory Standards Institute (CLSI); 2018. p. 64.
Shehata MG, Sohaimy SA, El-Sahn MA, Youssef MM. Screening of isolated potential probiotic lactic acid bacteria for cholesterol-lowering property and bile salt hydrolase activity. Ann Agric Sci. 2016;61:65-75. https://doi.org/10.1016/j.aoas.2016.03.001 DOI: https://doi.org/10.1016/j.aoas.2016.03.001
Azizi F, Najafi MB, Dovom MR. The biodiversity of Lactobacillus spp. from Iranian raw milk Motal cheese and antibacterial evaluation based on bacteriocin-encoding genes. AMB Express. 2017;7:1-10. https://doi.org/10.1186/s13568-017-0474-2 PMid:28921480 DOI: https://doi.org/10.1186/s13568-017-0474-2
Hu CH, Ren LQ, Zhou Y, Ye BC. Characterization of antimicrobial activity of three Lactobacillus plantarum strains isolated from Chinese traditional dairy food. Food Sci Nutr. 2019;7:1997-2005. https://doi.org/10.1002/fsn3.1025 PMid:31289647 DOI: https://doi.org/10.1002/fsn3.1025
Ansari JM, Colasacco C, Emmanouil E, Kohlhepp S, Harriott SO. Strain-level diversity of commercial probiotic isolates of Bacillus, Lactobacillus, and Saccharomyces species illustrated by molecular identification and phenotypic profiling. PLoS One. 2019;14:e0213841. https://doi.org/10.1371/journal.pone.0213841 PMid:30901338 DOI: https://doi.org/10.1371/journal.pone.0213841
Pérez-Díaz IM, Johanningsmeier SD, Anekella K, Pagán-Medina CG, Méndez-Sandoval L, Arellano C, et al. Genotypic and phenotypic diversity among Lactobacillus plantarum and Lactobacillus pentosus isolated from industrial scale cucumber fermentations. Food Microbiol. 2021;94:103652. https://doi.org/10.1016/j.fm.2020.103652 PMid:33279077 DOI: https://doi.org/10.1016/j.fm.2020.103652
Flórez AB, Mayo AO. Genome analysis of Lactobacillus plantarum LL441 and genetic characterisation of the locus for the lantibiotic plantaricin C. Front Microbiol. 2018;9:1916. https://doi.org/10.3389/fmicb.2018.01916 PMid:30174666 DOI: https://doi.org/10.3389/fmicb.2018.01916
Suzuki S, Fujita K, Maeno S, Shiwa Y, Endo A, Yokota K, et al. PCR-based screening, isolation, and partial characterization of motile lactobacilli from various animal feces. BMC Microbiol. 2020;20:1-11. https://doi.org/10.1186/s12866-020-01830-7 PMid:32493209 DOI: https://doi.org/10.1186/s12866-020-01830-7
Rocha J, Botelho J, Ksiezarek M, Perovic SU, Machado M, Carriço JA, et al. Lactobacillus mulieris sp. nov., a new species of Lactobacillus delbrueckii group. Int J Syst Evol Microbiol. 2020;70:1522-7. https://doi.org/10.1099/ijsem.0.003901 PMid:31951193 DOI: https://doi.org/10.1099/ijsem.0.003901
Tohno M, Tanizawa Y, Irisawa T, Masuda T, Sakamoto M, Arita M, et al. Lactobacillus silagincola sp. nov. and Lactobacillus pentosiphilus sp. nov., isolated from silage. Int J Syst Evol Microbiol. 2017;67:3639-44. https://doi.org/10.1099/ijsem.0.002196 PMid:28879844 DOI: https://doi.org/10.1099/ijsem.0.002196
Goel A, Halami PM, Tamang JP. Genome analysis of Lactobacillus plantarum isolated from some Indian fermented foods for bacteriocin production and probiotic marker genes. Front Microbiol. 2020;11:40-52. https://doi.org/10.3389/fmicb.2020.00040 PMid:32063893 DOI: https://doi.org/10.3389/fmicb.2020.00040
Prete R, Long SL, Joyce SA, Corsetti A. Genotypic and phenotypic characterization of food-associated Lactobacillus plantarum isolates for potential probiotic activities. FEMS Microbiol Lett. 2020;367:fnaa076. https://doi.org/10.1093/femsle/fnaa076 PMid:32386211 DOI: https://doi.org/10.1093/femsle/fnaa076
Ahaotu NN, Echeta CK, Bede NE, Awuchi CG, Anosike CL, Ibeabuchi CJ, et al. Study on the nutritional and chemical composition of “Ricinus communis (Ogiri)” condiment made from sandbox seed (Hura crepitans) as affected by fermentation time. GSC Biol Pharm Sci. 2020;11:105-13. https://doi.org/10.30574/gscbps.2020.11.2.0115 DOI: https://doi.org/10.30574/gscbps.2020.11.2.0115
Guissou AW, Parkouda C, Anaïs CK, Korotimi T, Oboulbiga EB, Savadogo A. Fermentation effect on the nutrient and antinutrient composition of Senegalia macrostachya and Parkia biglobosa seeds: A comparative study. Food Nutr Sci. 2020;11:726-40. https://doi.org/10.4236/fns.2020.117052 DOI: https://doi.org/10.4236/fns.2020.117052
Ollo K, Abel BZ, Mathurin YK, Pascale AD, Rose KN. Microbiological Quality of “Soumbala”, an African Locust Bean (Parkia biglobosa) Condiment Sold in the Markets of Abidjan, Côte d’Ivoire. J Adv Microbiol. 2020;20:67-74. https://doi.org/10.9734/jamb/2020/v20i1030291 DOI: https://doi.org/10.9734/jamb/2020/v20i1030291
Oloyede GK, Akintunde TI. Fatty acids profile, physicochemical properties and antioxidant activity of unfermented and fermented Parkia biglobosa (African Locust beans) seed oil. J Chem Soc Nigeria. 2019;44:178-86.
Olagunju OF, Ezekiel OO, Ogunshe AO, Oyeyinka SA, Ijabadeniyi OA. Effects of fermentation on proximate composition, mineral profile and antinutrients of tamarind (Tamarindus indica L.) seed in the production of daddawa-type condiment. LWT. 2018;90:455-9. https://doi.org/10.1016/j.lwt.2017.12.064 DOI: https://doi.org/10.1016/j.lwt.2017.12.064
Okwunodulu IN, Agha EF. Nutritional properties of indigenous fermented condiment (Ricinus communis (Ogiri)) produced from partial substitution of castor oil bean (Ricinus communis) with soybean (Glycine max) seeds. Niger J Biotechnol. 2020;37:32-46. https://doi.org/10.4314/njb.v37i2.4 DOI: https://doi.org/10.4314/njb.v37i2.4
Tersoo-Abiem EM, Sule S, Iwuamadi I, Awulu EO. Quality evaluation of dried fermented locust bean and soybean condiments. Eur J Agric Food Sci. 2021;3:63-7. https://doi.org/10.24018/ejfood.2021.3.2.261 DOI: https://doi.org/10.24018/ejfood.2021.3.2.261
Uzodinma EO, Okoyeuzu CF, Uchegbu NN, Okpala CO, Rasaq W, Shorstkii I, et al. Cubing fabrication/costing and machine performance on African fermented condiment quality attributes compared with commercial bouillon types. Processes. 2021;9:481-501. https://doi.org/10.3390/pr9030481 DOI: https://doi.org/10.3390/pr9030481
Compaorà CS, Tapsoba FW, Parkouda C, Tamboura DE, Traorà EM, Diawara BE, et al. Development of starter cultures carrier for the production of high quality soumbala, a food condiment based on Parkia biglobosa seeds. Afr J Biotechnol. 2020;19:820-8. https://doi.org/10.5897/AJB2020.17244 DOI: https://doi.org/10.5897/AJB2020.17244
Huang CH, Li SW, Huang L, Watanabe K. Identification and classification for the Lactobacillus casei group. Front Microbiol. 2018;9:1974. https://doi.org/10.3389/fmicb.2018.01974 PMid:30186277 DOI: https://doi.org/10.3389/fmicb.2018.01974
Jitpakdee J, Kantachote D, Kanzaki H, Nitoda T. Selected probiotic lactic acid bacteria isolated from fermented foods for functional milk production: Lower cholesterol with more beneficial compounds. LWT. 2021;135:110061. https://doi.org/10.1016/j.lwt.2020.110061 DOI: https://doi.org/10.1016/j.lwt.2020.110061
Das S, Mishra BK, Hati S. Techno-functional characterization of Indigenous Lactobacillus isolates from the traditional fermented foods of Meghalaya, India. Curr Res Food Sci. 2020;3:9-18. https://doi.org/10.1016/j.crfs.2020.01.002 PMid:32914116 DOI: https://doi.org/10.1016/j.crfs.2020.01.002
Priyanka TR, Kanagam N, Narayanan RB. Isolation and characterization of the probiotic potential of Lactobacillus species from Zingiber officinale. Int J Eng Sci Technol. 2019;7:173-7. https://doi.org/10.33564/IJEAST.2019.v04i07.028 DOI: https://doi.org/10.33564/IJEAST.2019.v04i07.028
Seddik HA, Bendali F, Gancel F, Fliss I, Spano G, Drider D. Lactobacillus plantarum and its probiotic and food potentialities. Probiotics Antimicrob Proteins. 2017;9:111-22. https://doi.org/10.1007/s12602-017-9264-z PMid:28271469 DOI: https://doi.org/10.1007/s12602-017-9264-z
Thakkar PN, Patel A, Modi HA, Prajapati JB. Hypocholesterolemic effect of potential probiotic Lactobacillus fermentum strains isolated from traditional fermented foods in wistar rats. Probiotics Antimicrob Proteins. 2020;12:1002-11. https://doi.org/10.1007/s12602-019-09622-w PMid:31760594 DOI: https://doi.org/10.1007/s12602-019-09622-w
Adesulu-Dahunsi AT, Sanni AI, Jeyaram K, Banwo K. Genetic diversity of Lactobacillus plantarum strains from some indigenous fermented foods in Nigeria. LWT. 2017;82:199-206. https://doi.org/10.1016/j.lwt.2017.04.055 DOI: https://doi.org/10.1016/j.lwt.2017.04.055
Bengoa AA, Iraporda C, Acurcio LB, de Cicco Sandes SH, Costa K, Guimarães GM, et al. Physicochemical, immunomodulatory and safety aspects of milks fermented with Lactobacillus paracasei isolated from kefir. Int Food Res J. 2019;123:48-55. https://doi.org/10.1016/j.foodres.2019.04.041 PMid:31284997 DOI: https://doi.org/10.1016/j.foodres.2019.04.041
Sharma S, Kandasamy S, Kavitake D, Shetty PH. Probiotic characterization and antioxidant properties of Weissella confusa KR780676, isolated from an Indian fermented food. LWT. 2018;97:53-60. https://doi.org/10.1016/j.lwt.2018.06.033 DOI: https://doi.org/10.1016/j.lwt.2018.06.033
Sornsenee P, Singkhamanan K, Sangkhathat S, Saengsuwan P, Romyasamit C. Probiotic properties of Lactobacillus species isolated from fermented palm sap in Thailand. Probiotics Antimicrob Proteins. 2021;1:1-13. https://doi.org/10.1007/s12602-021-09754-y PMid:33595830 DOI: https://doi.org/10.1007/s12602-021-09754-y
Ali F, Zayed G, Saad OA, Gharib SA. Antimicrobial activity and probiotic properties of lactic acid bacteria isolated from traditional fermented dairy products. J Mod Sci. 2020;32:40-8. https://doi.org/10.21608/JMR.2020.22931.1015 DOI: https://doi.org/10.21608/jmr.2020.22931.1015
Mulaw G, Sisay Tessema T, Muleta D, Tesfaye A. In vitro evaluation of probiotic properties of lactic acid bacteria isolated from some traditionally fermented Ethiopian food products. Int J Microbiol. 2019;2019:7179514. https://doi.org/10.1155/2019/7179514 PMid:31534458 DOI: https://doi.org/10.1155/2019/7179514
Ahmad A, Yap WB, Kofli NT, Ghazali AR. Probiotic potentials of Lactobacillus plantarum isolated from fermented durian (Tempoyak), a Malaysian traditional condiment. Nutr Food Sci. 2018;6:1370-7. https://doi.org/10.1002/fsn3.672 PMid:30258578 DOI: https://doi.org/10.1002/fsn3.672
Nath S, Sikidar J, Roy M, Deb B. In vitro screening of probiotic properties of Lactobacillus plantarum isolated from fermented milk product. Food Qual Saf. 2020;4:213-23. https://doi.org/10.1093/fqsafe/fyaa026 DOI: https://doi.org/10.1093/fqsafe/fyaa026
Okorie PC, Olasupo NA, Anike FN, Elemo GN, Isikhuemhen OS. Incidence of enteric pathogens in ugba, a traditional fermented food from African oil bean seeds (Pentaclethra macrophylla). Int J Food Conta. 2017;4:1-8. https://doi.org/10.1186/s40550-017-0057-7 DOI: https://doi.org/10.1186/s40550-017-0057-7
Devi SM, Kurrey NK, Halami PM. In vitro anti-inflammatory activity among probiotic Lactobacillus species isolated from fermented foods. J Funct Foods. 2018;47:19-27. https://doi.org/10.1016/j.jff.2018.05.036 DOI: https://doi.org/10.1016/j.jff.2018.05.036
Ojewumi ME. Effects of salting and drying on the deterioration rate of fermented Parkia biglobosa seed. J Nutr Health Food Eng. 2018;8:1-5. https://doi.org/10.15406/jnhfe.2018.08.00253 DOI: https://doi.org/10.15406/jnhfe.2018.08.00253
Sarmurzina Z, Bissenova G, Zakarya K, Dospaeva R, Shaikhin S, Abzhalelov A. Characterization of probiotic strains of Lactobacillus candidates for development of synbiotic product for Kazakh population. J Pure Appl Microbiol. 2017;11:151-61. https://doi.org/10.22207/JPAM.11.1.20 DOI: https://doi.org/10.22207/JPAM.11.1.20
Yao W, Yang L, Shao Z, Xie L, Chen L. Identification of salt tolerance-related genes of Lactobacillus plantarum D31 and T9 strains by genomic analysis. Ann Microbiol. 2020;70:1-14. https://doi.org/10.1186/s13213-020-01551-2 DOI: https://doi.org/10.1186/s13213-020-01551-2
Ademola OM, Adeyemi TE, Ezeokoli OT, Ayeni KI, Obadina AO, Somorin YM, et al. Phylogenetic analyses of bacteria associated with the processing of iru and ogiri condiments. Lett Appl Microbiol. 2018;67:354-62. https://doi.org/10.1111/lam.13040 PMid:29947432 DOI: https://doi.org/10.1111/lam.13040
Adesulu-Dahunsi AT, Dahunsi SO, Olayanju A. Synergistic microbial interactions between lactic acid bacteria and yeasts during production of Nigerian indigenous fermented foods and beverages. Food Control. 2020;110:106963. https://doi.org/10.1016/j.foodcont.2019.106963 DOI: https://doi.org/10.1016/j.foodcont.2019.106963
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