Abstract
Screening and molecular identification of probiotic lactic acid bacteria (LAB) in effluents generated during the production of ogi, a fermented cereal (maize, millet, and sorghum) were done. LAB were isolated from effluents generated during the first and second fermentation stages in ogi production. Bacterial strains isolated were identified microscopically and phenotypically using standard methods. Probiotic potential properties of the isolated LAB were investigated in terms of their resistance to pH 1.5 and 0.3% bile salt concentration for 4 h. The potential LAB isolates ability to inhibit the growth of pathogenic organisms (Escherichia coli, Staphylococcus aureus, and Salmonella typhimurium) was evaluated in vitro. The pH and LAB count in the effluents ranged from 3.31 to 4.49 and 3.67 to 4.72 log cfu/ml, respectively. A total of 88 LAB isolates were obtained from the effluents and only 10 LAB isolates remained viable at pH 1.5 and 0.3% bile salt. The zones of inhibition of the LAB isolates with probiotic potential ranged from 7.00 to 24.70 mm against test organsisms. Probiotic potential LAB isolates were molecularly identified as Lactobacillus plantarum, Lactobacillus fermentum, Lactobacillus reuteri, Enterococcus faecium, Pediococcus acidilactici, Pediococcus pentosaceus, Enterococcus faecalis, and Lactobacillus brevis. Survival and proliferation of LAB isolates at low pH, 0.3% bile salt condition, and their inhibition against some test pathogens showed that these LAB isolates could be a potential probiotics for research and commercial purposes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdollahzadeh E, Rezaei M, Hosseini H (2014) Antibacterial activity of plant essential oils and extracts: the role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control 35(1):177–183. https://doi.org/10.1016/j.foodcont.2013.07.004
Adebayo CO, Aderiye BI (2007) Ecology and antibacteria potential of lactic acid bacteria associated with cereals and cassava. Res J Microbiol 2:426–435. https://doi.org/10.3923/jm.2007.426.435
Adebayo-tayo BC, Onilude AA (2008) Screening of lactic acid bacteria strains isolated from some Nigerian fermented foods for EPS production. World Appl Sci J 4:741–747
Aderiye JB, Laleye SA (2004) Relevance of fermented food products in southwest Nigeria. Plant Foods Hum Nutr 58:1–16. https://doi.org/10.1023/B:QUAL.0000040315.02916.a3
Adiguzel GC, Atasever M (2009) Phenotypic and genotypic characterization of lactic acid bacteria isolated from Turkish dry fermented sausage. Rom Biotechnol Lett 14(1):4130–4138
Adnan A, Tan I (2006) Isolation of lactic acid bacteria from Malaysian foods and assessment of the isolates for industrial potential. Bioresour Technol 98:1380–1385. https://doi.org/10.1016/j.biortech.2006.05.034
Argyri AA, Zoumpopolou G, Karatzas KA, Tsakalidou E, Nychas GE, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291. https://doi.org/10.1016/j.fm.2012.10.005
Ashe B, Paul S (2010) Isolation and characterization of lactic acid bacteria from dairy effluents. J Environ Res Dev 4(4):983–991
Aslam S, Qazi JI (2010) Isolation of acidophilic lactic acid bacteria antagonistic to microbial contaminants. Pak J Zool 42(5):567–573
Ayodeji BD, Clara FP, Vincenza AW, Moreira PR, Obadina AO, Sanni LO, Pintado MM (2017) Screening and molecular identification of lactic acid bacteria from gari and fufu and gari effluents. Ann Microbiol 67:123–133. https://doi.org/10.1007/s13213-016-1243-1
Banigo EB, Akpapunam MA (1987) Physicochemical and nutritional evaluation of protein enriched fermented maize flours. Niger Food J 5:30–36
Banwo K, Sanni A, Tan H, Tian Y (2012) Phenotypic and genotypic characterization of lactic acid bacteria isolated from some Nigerian traditional fermented food. Food Biotechnol 26:124–142. https://doi.org/10.1080/08905436.2012.670831
Bhattacharyya BK (2009) Emergence of probiotics in therapeutic applications. Int J Pharm Sci Nanotechnol 2(1):383–389. https://doi.org/10.1021/jf021150r
Bolaji OT, Adenuga-Ogunji L, Abegunde TA (2017) Optimization of processing conditions of ogi produced from maize using response surface methodology (RSM). Cogent Food Agric 3(1407279). https://doi.org/10.1080/23311932.2017.1407279
Bulut C (2003) Isolation and molecular characterization of lactic acid bacteria from cheese. Dissertation. Izmir Institute of Technology
Cabo ML, Braber AF, Koenraad PM (2002) Apparent antifungal activity of several lactic acid bacteria against Penicillium discolour is due to acetic acid in the medium. J Food Prot 65(8):1309–1316. https://doi.org/10.4315/0362-028X-65.8.1309
Chapman CM, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixture more effective than single strains. Eur J Nutr 50:1–17. https://doi.org/10.1007/s00394-010-0166-z
Corona F, Martinez JL (2013) Phenotypic resistance to antibiotics. Antibiotics 2(2):237–255. https://doi.org/10.3390/antibiotics2020237
Dike KS, Sanni AI (2010) Influence of starter culture of lactic acid bacteria on the shelf life of agidi; an indigenous fermented cereal product. Afr J Biotechnol 9:7922–7927. https://doi.org/10.5897/AJB09.1203
Draksler D, Gonzales S, Oliver G (2004) Preliminary assays for the development of a probiotic for goats. Reprod Nutr Dev 44:397–405. https://doi.org/10.1051/rnd:2004046
Fernández L, Hancock RE (2012) Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev 25(4):661–681. https://doi.org/10.1128/CMR.00043-12
Gotcheva V, Hristozova E, Hristozova T, Guo M, Roshkova Z, Angelov A (2002) Assessment of potential probiotic properties of lactic acid bacteria and yeast strains. Food Biotechnol 16:211–225. https://doi.org/10.1016/j.foodcont.2013.09.044
Grosu-Tudor SS, Stancu MM, Pelinescu D, Zamfir M (2014) Characterization of some bacteriocins produced by lactic acid bacteria isolated from fermented foods. World J Microbiol Biotechnol 30:2459–2469. https://doi.org/10.1007/s11274-014-1671-7
Haller D, Colbus H, Ganzle MG, Scherenbacher P, Bode C, Hammes WP (2001) Metabolic and functional properties of lactic acid bacteria in the gastro-intestinal ecosystem: a comparative in vitro study between bacteria of intestinal and fermented food origin. Syst Appl Microbiol 24:218–226. https://doi.org/10.1078/0723-2020-00023
Hoque MZ, Akter F, Hossain KM, Rahman MS, Billah MM, Islam KM (2010) Isolation, identification and analysis of probiotic properties of Lactobacillus spp. from selective regional yoghurts. World J Dairy Food Sci 5(1):39–46
Ijabadeniyi AO (2007) Microorganisms associated with ogi traditionally produced from three varieties of maize. Res J Microbiol 2:247–253. https://doi.org/10.3923/jm.2007.247.253
Iranmanesh M, Ezzatpanah H, Mojgani N (2014) Antibacterial activity and cholesterol assimilation of lactic acid bacteria isolated from traditional Iranian dairy products. LWT Food Sci Technol 58:355–359. https://doi.org/10.1016/j.lwt.2013.10.005
Kailasapathy K, Chin J (2000) Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 78:80–88. https://doi.org/10.1046/j.1440-1711.2000.00886.x
Klaenhammer T, Kullen M (1999) Selection and design of probiotics. Int J Food Microbiol 50:45–47
Korhonen J (2010) Antibiotic resistance of lactic acid bacteria. dissertation, University of Eastern Finland
Kostinek M, Pukall R, Rooney AP, Schillinger U, Hertel C, Holzapfel WH, Franz CM (2005) Lactobacillus arizonensis is a later heterotypic synonym of Lactobacillus plantarum. Int J Syst Evol Microbiol 55:2485–2489. https://doi.org/10.1099/ijs.0.63880-0
Kuda T, Kawahara M, Nemoto M, Takahashi H, Kimura B (2014) In vitro antioxidant and anti-inflammation properties of lactic acid bacteria isolated from fish intestines and fermented fish from the Sanriku Satoumi region in Japan. Food Res Int 64:248–255. https://doi.org/10.1016/j.foodres.2014.06.028
Lawalata HJ, Sembiring L, Rahayu ES (2011) Molecular identification of lactic acid bacteria producing antimicrobial agents from Bakasang, an Indonesian traditional fermented fish product. Indones. J Biotechnol 16(2):93–99
Lonkar P, Harne SD, Kalorey DR, Kurkure NV (2005) Isolation, in vitro antibacterial activity, bacterial sensitivity and plasmid profile of Lactobacilli. Asian Australas J Anim Sci 18(9):1336–1342
Messi P, Bondi M, Sabia C, Battini R, Manicardi G (2001) Detection and preliminary characterization of a bacteriocin (plantaricin 35d) produced by a Lactobacillus plantarum strain. Int J Food Microbiol 64:193–198
Millette M, Smoragiewicz W, Lacroix M (2004) Antimicrobial potential of immobilized Lactococcus lactis sub sp lactis ATCC 11454 on selected bacteria. J Food Prot 67(6):1184–1189. https://doi.org/10.4315/0362-028X-67.6.1184
Mohania D, Nagpal R, Kumar M, Bhardwaj A, Yadav M, Jain S, Marotta F, Singh V, Parkash OM, Yadav H (2008) Molecular approaches for identification and characterization of lactic acid bacteria. J Dig Dis 9:190–198. https://doi.org/10.1111/j.1751-2980.2008.00345.x
Odunfa SA, Adeyele S (1985) Microbiological changes during the traditional production of ogi baba, a West African fermented sorghum gruel. J Cereal Sci 3:173–180. https://doi.org/10.1016/S0733-5210(85)80027-8
Oguntoyinbo FA, Narbad A (2012) Molecular characterization of lactic acid bacteria and in situ amylase expression during traditional fermentation of cereal foods. Food Microbiol 31:254–262. https://doi.org/10.1016/j.fm.2012.03.004
Omafuvbe B, Esosuakpo E, Oladejo T, & Toye A (2007) Effect of soaking and roasting dehulling methods of soybean on Bacillus fermentation of soy-daddawa. Am. J. Food Technol, 2(257.264). https://doi.org/10.3923/ajft.2007.257.264
Omemu AM (2011) Assessment of the antimicrobial activity of lactic acid bacteria isolated from two fermented maize products—ogi and kunnu-zaki. Malays J Microbiol 7:124–128. https://doi.org/10.21161/mjm.25710
Onyekwere OO, Akinrele IA, Koleoso OA (1989) Industrialization of ogi fermentation. In: Steinkraus (ed) Industrialization of indigenous fermented foods, 3rd edn. Marcel Dekker, New-York, pp 329–362
Oranusi SU, Umoh VJ, Kwaga JP (2003) Hazards and critical control points of Kunun Zaki, a non-alcoholic beverage in northern Nigeria. Food Microbiol 20:127–132. https://doi.org/10.1016/S0740-0020(02)00072-2
Oyedeji O, Onilude AA, Ogunbanwo ST (2013) Predominant lactic acid bacteria involved in the traditional fermentation of fufu and ogi, two Nigerian products. Food Nutr Sci 4:40–46. https://doi.org/10.4236/fns.2013.411A006
Oyewole OA, Isah P (2012) Locally fermented foods in Nigeria and their significance to national economy: a review. J Rec Adv Agric 1(4):92–102
Rolfe RD (2000) The role of probiotic cultures in the control of gastrointestinal health. J Nutr 130:3965–3980. https://doi.org/10.1093/jn/130.2.396S
Saarela M, Lathenmaki L, Crittenden R, Salminen S, Mattilasandholm T (2002) Gut bacteria and health foods—the European perspective. Int J Food Microbiol 78:99–117. https://doi.org/10.1016/S0168-1605(02)00235-0
Salminen S, Von Wright A (1998) Current probiotics—safety assured? Microb Ecol Health Dis 10:68–77
Sanni A, Franz C, Schillinger U, Huch M, Guigas C, Holzapfel W (2013) Characterization and technological properties of lactic acid bacteria in the production of yorghurt. A cereal-based product. Food Biotechnol 27:178–198. https://doi.org/10.1080/08905436.2013.781949
Sarkono M, Rahman F, Sofyan Y (2010) Isolation and identification of lactic acid bacteria from abalone (Haliotis asinina) as a potential candidate of probiotic. Bioscience 2(1):38–42. https://doi.org/10.13057/nusbiosci/n020106
Sathyabama S, Ranjith Kumar M, Bruntha devi P, Vijayabharathi R, Brindha Priyadharisini V (2014) Co-encapsulation of probiotics with prebiotics on alginate matrix and its effect on viability in simulated gastric environment. LWT–Food Sci Technol 57:419–425. https://doi.org/10.1016/j.lwt.2013.12.024
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. https://doi.org/10.1016/j.fm.2013.10.003
Steinkraus KH (1996) Indigenous fermented foods involving an acid fermentation. In: Steinkraus (ed) Handbook of indigenous fermented foods, 2nd edn. Marcel Dekker, New York, pp 111–347
Tambekar DH, Bhutada SA (2010) Studies on antimicrobial activity and characteristics of bacteriocins produced by Lactobacillus strains isolated from milk of domestic animals. Int J Microbiol 8:1–6
Teniola OD, Odunfa SA (2002) Microbial assessment and quality evaluation of ogi during spoilage. World J Microbiol Biotechnol 18:731–737. https://doi.org/10.1023/A:1020426304881
Teniola OD, Holzapfel WH, Odunfa SA (2005) Comparative assessment of fermentation techniques useful in the processing of ogi. World J Microbiol Biotechnol 21:39–43. https://doi.org/10.1007/s11274-004-1549-1
Ukeyima MT, Enujiugha VN, Sanni TA (2010) Current applications of probiotic foods in Africa. Afr J Biotechnol 9:394–401
Vandenberg PA (1993) Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol Rev 12:221–238. https://doi.org/10.1111/j.1574-6976.1993.tb00020.x
Acknowledgments
The authors thank the Department of Food Science and Technology, FUNAAB and Dr. Obadina for their immense contribution towards the success of the research project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Rights and permissions
About this article
Cite this article
Olatunde, O.O., Obadina, A.O., Omemu, A.M. et al. Screening and molecular identification of potential probiotic lactic acid bacteria in effluents generated during ogi production. Ann Microbiol 68, 433–443 (2018). https://doi.org/10.1007/s13213-018-1348-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-018-1348-9