DIVERSITY OF BACILLUS SPECIES AND THEIR ANTIMICROBIAL COMPOUNDS INVOLVED IN ALKALINE-FERMENTATION OF INDIGENOUS FOOD CONDIMENTS USED IN AFRICA.
- Laboratory of Biotechnology in Food and Nutritional Sciences, Research Center in Biological Food and Nutritional Sciences, Department of Biochemistry and Microbiology, Research and Training Unit in Life and Earth Sciences, University Ouaga I, Prof. Joseph KI-ZERBO, 03 B.P 7031 Ougadougou 03,Burkina Faso.
- Department of Microbiology, Faculty of Biological Sciences, University of Nigeria Nsukka, 410001, Enugu state, Nigeria.
- Abstract
- Keywords
- References
- Cite This Article as
- Corresponding Author
The indigenous food condiments, produced by alkaline fermentation of various African plant products, are widely used as food seasonings by most African people. Many strains of Bacillus genus are recognized as dominant microorganisms responsible of bioconversion of diverse plant-based seeds for the production of African alkaline-fermented food condiments. The involved Bacillus strains are known to produce a wide arsenal of useful antimicrobial compounds, particular polypeptides, lipopeptides and bacteriocins that exert broader spectra activities against Gram-negative and Gram-positive bacteria and fungi implicated in food toxicity or spoilage and ultimately human pathogenicity. Lipopeptides and bacteriocins present diverse biochemical structures with different mode and mechanism of action linked to their genetic and biosynthesis pathway. The molecular biology methods currently use in microbiological research allowed more reliable identification of antimicrobial polypeptides-producing Bacillus strains from these foods generating sufficient knowledge which potentiated the selection of starters cultures. The starters cultures and their antimicrobial peptides know a growing interest for effectiveness and best applications in many life domains. In this review, current knowledge about the main Bacillus species involved in African alkaline-fermented food condiments processes, mode and mechanism of action, genetic and biosynthesis pathway, and food applications of the antimicrobial peptides produced by these Bacillus strains are discussed.
- Abaelu, A.M., Olukoya, D.K., Okochi, VI., and Akinrimisi E.O. (1990): Biochemical changes in fermented Melon Egusi, seeds Citrullis Vulgaris. J. Industrial Microbiol., 6: 211?214.
- Abriouel, H., Franz, C.M.A.P., Omar, N. B., and G?lvez A. (2011): Diversity and applications of Bacillus bacteriocins. FEMS Microbiol. Rev. 35(1): 201?232. doi:10.1111/j.1574-576 6976.2010.00244.
- Ahern M., Verschueren, S., and van Sinderen D. (2003): Isolation and Characterization of a novel bacteriocin produced by Bacillus thuringiensis strain B439. FEMS Microbiol. Lett., 163: 229?236.
- Akpa, E., Jacques P., Wathelet B. et al. (2001): Influence of culture conditions on lipopeptide production by Bacillus subtilis. Appl. Biochem. and Biotechnol. -Part A Enzy. Engin. Biotechnol., 91(93): 551?561.
- Altena, K., Guder, A., Cramer, C., and Bierbaum, G. (2000): Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster. Appl. Environ. Microbiol., 66: 2565?2571.
- Alvarez-Sieiro, P., Montalb?n-L?pez, M., Mu, D., and Kuipers, O.P. (2016): Bacteriocins of lactic acid bacteria: extending the family. Appl. Microbiol. Biotechnol., 100: 2939?2951. doi: 10.1007/s00253-016-7343-9
- Aranda, F. J., Teruel, J.A., and Ortiz, A. (2005): Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochimica et Biophysica Acta-Biomembranes., 1713(1): 51?56.
- Arias, A.A., Ongena, M., Devreese, B., Terrak, M., Jiri?s, B., and Fickers, P. (2013): Characterization of amylolysin, a novel lantibiotic from Bacillus amyloliquefaciens GA1. PLOS One. 8: e83037. doi: 10.1371/journal.pone.0083037.
- Arnison, P. G., Bibb, M. J., Bierbaum, G., Bowers, A. A., Bugni, T. S., Bulaj, G., et al. (2013): Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat. Prod. Rep., 30: 108-160.doi: 10.1039/c2np20085f.
- Aron, Z.D. et al. (2005): Characterization of a new tailoring domain in polyketide biogenesis: The amine transferase domain of MycA in the mycosubtilin gene cluster. J. Am. Chem. Soc., 127: 14986?14987.
- Azokpota, P., Hounhouigan, D. J, Nago, M.C., and Jakobsen M. (2006): Esterase and protease activities of Bacillus spp. from afitin, iru and sonru: three African locust bean (Parkia biglobosa) condiments from Benin. African J. Biotechnol., 5(3): 265 ? 272.
- Azokpota, P., Hounhouigan, D.J., Annan, N.T., Nago, M.C., and Jakobsen M. (2008): Diversity of volatile compounds of afitin, iru and sonru, three fermented food condiments from Benin. World J. Microbiol. Biotechnol., 24: 879?885.
- Babasaki, K., Takao, T., Shimonishi, Y., and Kurahashi, K. (1985). Subtilosin A, a new antibiotic peptide produced by Bacillus subtilis 168: isolation, structural analysis, and biogenesis. J. Biochem. (Tokyo)., 98(3): 585 ? 603. PMID:3936839.
- Baindara, P., Mandal, S.M., Chawla, N., Singh, P.K., Pinnaka, A.K., and Korpole, S. (2013). Characterization of two antimicrobial peptides produced by a halotolerant Bacillus subtilis strain SK.DU.4 isolated from a rhizosphere soil sample. AMB Express., 3(1): 2. doi:10.1186/2191-0855-3-2.
- Barbosa, T.M., Serra, C.R., La Ragione, R.M., Woodward, M.J., and Henriques A.O. (2005). Screening for Bacillus isolates in the broiler gastrointestinal tract. Appl. Environ. Microbiol., 71: 968?978.
- Begley, M., Cotter, P.D., Hill, C., and Ross, R.P. (2009): Identification of a Novel Two-Peptide Lantibiotic, Lichenicidin, following Rational Genome Mining for LanM Proteins. Appl. Environ. Microbiol., 75: 5451?5460.
- Belguesmia, Y., Naghmouchi, K., Chihib, N.E., and Drider, D. (2011): Class IIa bacteriocins: current knowledge and perspectives. In Drider D et Rebuffat S (Ed.), Prokaryotic antimicrobial peptides: From genes to applications. New York: Springer, p171?195. doi: http://dx.doi.org/10.1007/978-1-4419-7692-5_10.
- Bierbaum, G., and Sahl, H.G. (2009): Lantibiotics: mode of action, biosynthesis and bioengineering. Curr. Pharm. Biotechno.,10: 2-18.
- Bierbaum, G., Br?tz, H., Koller, K.P., and Sahl, H.G. (1995): Cloning, sequencing and production of the lantibiotic mersacidin. FEMS Microbiol. Lett., 127: 121?126.
- Br?tz, H., Bierbaum, G., Leopold, K., Reynolds, P.E., and Sahl, H.G. (1998): The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob. Agents. Ch., 42: 154?160.
- Chatterjee, C., Paul, M., Xie, L., and van der Donk, W.A. (2005): Biosynthesis and mode of action of lantibiotics. Chem. Rev.,105: 633?684.
- Chatterjee, S., Chatterjee, S., Lad, S.J., Phansalkar, M.S., Rupp, R.H., Ganguli, B.N., Fehlhaber, H.W., and Kogler, H. (1992): Mersacidin, a new antibiotic from Bacillus. Fermentation, isolation, purification and chemical characterization. J. Antibiot. (Tokyo)., 45(6): 832-838. doi:10.7164/antibiotics.45.832.
- Chehimi, S., Delalande, F., Sable, S., Hajlaoui, M.R., Van Dorsselaer, A., Limam, F., and Pons, A.M. (2007): Purification and partial amino acid sequence of thuricin S, a new anti-Listeria bacteriocin from Bacillus thuringiensis. Can. J. Microbiol., 53: 284?90.
- Chen, H., and Hoover, D.G. (2003): Bacteriocins and their food applications. Compr. Rev. Food Sci. Food Safety., 2(3): 82?100. doi: http://dx.doi.org/10.1111/j.1541-4337.2003.tb00016.x
- Compaore, C.S., Jensen, L. B., Diawara, B., Ou?draogo, G. A., Jakobsen, M., and Ouoba, L.I. I. (2013c): Resistance to antimicrobials and acid and bile tolerance of Bacillus spp. isolated from Bikalga, fermented seeds of Hibiscus sabdariffa. African J. Food Sci., 7(11): 408?414. doi: 10.5897/AJFS2013.1018.
- Compaor?, C.S., Nielsen, D. S., Ouoba, L.I.I., Berner, T. S., Nielsen, K. F., Sawadogo-Lingani, H., Diawara, B., Ou?draogo, G.A., Jakobsen, M., and Thorsen, L. (2013a): Co-production of surfactin and a novel bacteriocin by Bacillus subtilis subsp. subtilis H4 isolated from Bikalga, an African Alkaline Hibiscus sabdariffa seed fermented condiment. Int. J. Food Microbiol., 162: 297?307
- Compaor?, C.S., Nielsen, D.S., Sawadogo-Lingani, H., Berner, T.S., Nielsen, K.F, Adimpong, B.D., Diawara, B., Ouedraogo, G.A., Jakobsen, M., and Thorsen, L. (2013b): Bacillus amyloliquefaciens ssp. plantarum strains as potential protective starter cultures for the production of Bikalga, an alkaline fermented food. J. Appl. Microbiol., 115: 133?146.
- Cotter, P. D, Hill C., et Ross, R.P. (2005b): Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol., 3(10): 777?788. doi: http://dx.doi.org/10.1038/nrmicro1273.
- Cotter, P.D., Ross, R.P., and Hill, C. (2013): Bacteriocins-available alternative to antibiotics? Nat. Rev. Microbiol.,11(2): 95?105. doi :10.1038/nrmicro2937. PMID:23268227.
- Da Silva Sabo, S., Vitolo, M., Gonz?lez, J.M.D., and De Souza Oliveira, R.P. (2014): Overview of Lactobacillus plantarum as a promising bacteriocin producer among lactic acid bacteria. Food Res. Int., 64: 527?536. doi: 10.1016/j.foodres.2014.07.041.
- Dischinger, J., Josten, M., Szekat, C., Sahl, H. G., and Bierbaum, G. (2009): Production of the novel two-peptide lantibiotic lichenicidin by Bacillus licheniformis DSM 13. PLoS One., 4(8): e6788. doi: 10.1371/journal.pone.0006788.
- Dortu, C., and Thonart, P. (2009) : Les bact?riocines des bact?ries lactiques : caract?ristiques et int?r?ts pour la bioconservation des produits alimentaires. Biotechnologie Agronomie Soci?t? et Environnement., 13(1): 143?154.
- Dubois, J.Y.F., Kouwen, T.R.H.M., Schurich, A.K.C., Reis, C.R., Ensing, H.T., Trip, E.N., Zweers, J.C., and van Dijl, J.M. (2009): Immunity to the bacteriocin sublancin 168 is determined by the SunI (YolF) protein of Bacillus subtilis. Antimicrob. Agents Ch., 53: 651?661.
- EFSA (2008): The maintenance of the list of QPS microorganisms intentionally added to foods or feeds. Scientific opinion of thepanel on biological hazards. EFSA J., 923: 1? 48.
- Ejiofor, M.A.N., Oti, E., and Okafor, J.C. (1987): Studies on the fermentation of seeds of the African oil bean tree Pentaclethra macrophylla. Int. Tree Crops J., 4: 135?144.
- Eze, V. C., Onwuakor, C. E., and Ukeka, E. (2014): Proximate composition, biochemical and microbiological changes associated with fermenting African oil bean (Pentaclethra macrophylla Benth) seeds. Amer. J. Microbiol., 2: 674?681.
- Feng, G., Guron, G.K.P., Churey, J.J., and Worobo, R.W. (2009): Characterization of mundticin L, a class IIa anti-Listeria bacteriocin from Enterococcus mundtii CUGF08. App. Environ. Microb., 75(17): 5708?5713. doi: http://dx.doi.org/10.1128/AEM.00752-09.
- Fernandez, B. (2014) : Activit? biologique et impact sur le microbiote intestinal des bact?ries lactiques bact?riocinog?nes. PhD thesis, Universit? Laval, Qu?bec, 143p.
- Freire, D.M.G., Araujo, L.V.D., Kronemberger, F.D.A. et al. (2009): Innovation in Food Engineering, CRC Press, New York, NY, USA.
- G?lvez, A., Abriouel, H., L?pez, R.L., and Omar, N.B. (2007): Bacteriocin-based strategies for food bio-preservation. Int. J. Food Microbiol., 120: 51?70.
- Guder, A., Wiedemann, I. and Sahl H.G. (2000): Post-translationally modified bacteriocins: the lantibiotics. Biopolymers. 55: 62?73.
- He, Z., Kisla, D., Zhang, L., Yuan, C., Green-Church, K.B., and Yousef, A.E. (2007): Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic and polymyxin. Appl. Environ. Microbiol., 73: 168 ?178.
- He, Z., Yuan, C., Zhang, L., and Yousef, A.E. (2008): N-terminal acetylation in paenibacillin, a novel lantibiotic. FEBS Lett., 582: 2787?2792.
- Holo, H., Jeknic, Z., Daeschel M., Stevanovic S., and Nes, I.F. (2001): Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology., 147: 643?651.
- Hong, H.A., Duc le, H., and Cutting, S.M. (2005): The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev., 29: 813?835.
- Huang, T., Geng, H., Miyyapuram, V.R., Sit, C.S., Vederas, J.C., and Nakano, M.M. (2009): Isolation of a variant of subtilosin A with hemolytic activity. J. Bacteriol., 191(18): 5690?5696. doi:10.1128/JB.00541-09.
- Hwang, A. L., and Jeong H.K. (2012): Isolation of Bacillus amyloliquefaciens strains with antifungal activities from Meju. Prev. Nutr. Food Sci.,17: 64?70. http://dx.doi.org/10.3746/pnf.2012.17.1.064.
- Inatsu, Y, Nakamura, N, Yuriko, Y, Fushimi, T, Watanasiritum, L, and Kawamoto, S (2006): Characterization of Bacillus subtilis strains in Thua nao, a traditional fermented soybean food in Northern Thailand. Lett. Appl. Microbiol., 43: 237?242.
- Jasniewski, J. (2008). ?tude des m?canismes d'action de bact?riocines de la sous-classe IIa. PhD thesis, Nancy-Universit?, Nancy, 155p.
- Jones, E., Salin V., and Williams, G.W. (2005): Nisin and the market for commercial bacteriocins TAMRC Consumer and Product Research Report No. CP-01-05 (pp. 25). Texas: Texas A & M University.
- Kabore, D., Thorsen, L., Nielsen, S.D., Berner, S.T., Sawadogo-Lingani, H., Diawara, B., Dicko, H.M., Jakobsen, M., (2012): Bacteriocin formation by dominant aerobic spore formers isolated from traditional maari. Int. J. Food Microbiol., 154: 10?18.
- Kamoun, F., Fguira, I.B., Tounsi, A., Abdelkefi-Mesrati, L., Sanchis, V., Lereclus, D. and Jaoua S. (2009): Generation of mini-Tn10 transposon insertion mutant library of Bacillus thuringiensis for the investigation of genes required for its bacteriocin production. FEMS Microbiol. Lett., 294: 141?149.
- Khem R.M., and Shamsher S. K. (2015): Review Article. Lipopeptides as the Antifungal and Antibacterial Agents: Applications in Food Safety and Therapeutics. Res. Int., Volume 2015 : Article ID 473050, 9 pages. http://dx.doi.org/10.1155/2015/473050.
- Kim, P. I., Bai, H., Bai, D., et al. (2004): Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J. Appl. Microbiol., 97(5): 942?949.
- Kiss, A., Baliko, G., Csorba, A., Chuluunbaatar, T., Medzihradszky, K.F., and Alf?ldi, L. (2008): Cloning and characterization of the DNA region responsible for megacin A-216 production in Bacillus megaterium 216. J. Bacteriol.,190: 6448?6457.
- Kjos, M., Salehian, Z., Nes, I.F., and Diep, D.B. (2010): An extracellular loop of the mannose phosphotransferase system component IIC is responsible for specific targeting by class IIa bacteriocins. J. Bacteriol., 192(22): 5906?5913. doi: http://dx.doi.org/10.1128/JB.00777-10.
- Klaenhammer, T.R. (1993): Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev., 12(1-3): 39?86. doi:10.1016/0168-6445(93)90057-G.
- Korenblum, E., De Araujo, L.V., Guimaraes, C.R., et al. (2012): Purification and characterization of a surfactin-like molecule produced by Bacillus spp. H2O-1 and its antagonistic effect against sulfate reducing bacteria. BMC Microbiol.,12(1): 252.
- Kouwen, T.R., van der Goot, A., Dorenbos, R., Winter, T., Antelmann, H., Plaisier, M.C., Quax, W.J., van Dijl, J.M., and Dubois, J.Y. (2007): Thiol-disulphide oxidoreductase modules in the low-GC Gram-positive bacteria. Molecular Microbiology., 64: 984?999.
- Kuipers, A., Rink, R., and Moll, G.N. (2011): Genetics, biosynthesis, structure, and mode of action of lantibiotics. In Drider D et Rebuffat S (Ed.), Prokaryotic Antimicrobial Peptides: From Genes to Applications. New York: Springer, USA, p147?169. doi: http://dx.doi.org/10.1007/978-1-4419-7692-5_9.
- Lawton, E. M., Cotter, P. D., Hill, C., and Ross, R. P. (2007): Identification of a novel two-peptide lantibiotic, Haloduracin, produced by the alkaliphile Bacillus halodurans C-125. FEMS Microbiol. Lett., 267(1): 64?71. doi:10.1111/j.1574-6968.2006.00539.
- Le Marrec, C., Hyronimus, B., Bressollier, P., Verneuil, B., Urdaci, M.C. (2000): Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I4. Appl. Environ. Microbiol., 66: 5213?5220.
- Lee, H., Churey, J.J. and Worobo, R.W. (2009b): Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiol. Lett., 299: 205?213.
- Lee, KD, Gray., E.J, Mabood, F., Jung, W.J., Charles, T., Clark, S.R., Ly, A., Souleimanov, A., Zhou, X., and Smith D.L. (2009a): The class IId bacteriocin thuricin-17 increases plant growth. Planta., 229: 747?55.
- Maget-Dana, R., and Peypoux, F. (1994): Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology., 87(1-3): 151?74.
- Makhloufi, K.M. (2011). Caract?risation d'une bact?riocine produite par une bact?rie lactique Leuconostoc pseudomesenteroides isol?e du boza. PhD Thesis, Universit? Pierre et Marie Curie-Paris VI, Paris, 228p.
- Mandal, S.M., Barbosa A.E.A.D., and Franco, O. L. (2013): Lipopeptides in microbial infection control: scope and reality for industry. Biotechnol. Adv., 31(2): 338?345.
- Marahiel, M.A., and Essen, L.O. (2009): Non-ribosomal peptide synthetases: mechanistic and structural aspects of essential domains. Methods in Enzymology., 458: 337?351.
- Marx, R., Stein, T., Entian, K.D., and Glaser, S.J. (2001): Structure of the Bacillus subtilis peptide antibiotic subtilosin A determined by 1H-NMR and matrix assisted laser desorption/ionization time-of-flight mass spectrometry. J. Protein. Chem., 20(6): 501?506. PMID:11760125.
- McAuliffe, O., Ross, R.P. and Hill, C. (2001): Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol. Rev., 25: 285?308.
- McClerren, A.L., Cooper, L.E., Quan, C., Thomas, P.M., Kelleher, N.L., and van der Donk, W.A. (2006): Discovery and in vitro biosynthesis of haloduracin, a two-component lantibiotic. P. Natl. Acad. Sci. USA. 103: 17243?17248.
- Mills, S., Serrano, L., Griffin, C., O?connor, P.M., Schaad, G., Bruining, C., et al. (2011): Inhibitory activity of Lactobacillus plantarum LMG P-26358 against Listeria innocula when used as an adjunct starter in the manufacture of cheese. Microbial Cell Factories., 10, S7. doi: 10.1186/1475-2859-10-S1-S7.
- Motta, A.S., Cannavan, F.S., Tsai, S., Brandelli, A. (2007b): Characterization of a broad range antibacterial substance from a new Bacillus species isolated from Amazon basin. Arch. Microbiol., 188: 367?375.
- Motta, A.S., Flores, F.S., Souto, A.A., and Brandelli, A. (2008): Antibacterial activity of a bacteriocin-like substance produced by Bacillus spp. P34 that targets the bacterial cell envelope. Antonie. Van Leeuwenhoek., 93(3): 275?284. doi:10.1007/s10482-007-9202-2.
- Nakano, M.M., Zheng, G., and Zuber, P. (2000): Dual control of sbo-alb operon expression by the Spo0 and ResDE systems of signal transduction under anaerobic conditions in Bacillus subtilis. J. Bacteriol., 182: 3274?3277.
- Nath S., Chowdhury S., and K.C. Dora. (2015): Application of Bacillus spp. as a biopreservative for food preservation. Journal of Engineering Research and Applications., ISSN: 2248-9622, 5(4): 85-95.
- Ndir, B., Hbid, C., Cornelius, C., Roblain, D., Jacques, P., Vanhentenryck, F., Diop, M., and Thonart, P. (1994). Propri?t?s antifongiques de la microflore sporul?e du n?t?tu. Cahiers Agricultures., 3 : 23?30.
- Nes, I.F., Yoon S.S., and Diep, D.B. (2007): Ribosomally synthesized antimicrobial peptides (bacteriocins) in lactic acid bacteria: a review. Food Sci. Biotechnol., 16: 675?690.
- Nicholson, W. (2002): Roles of Bacillus endospores in the environment. Cell. Mol. Life Sci. 59(3): 410?416. doi: http://dx.doi.org/10.1007/s00018-002-8433-7.
- Noll, K.S., Sinko, P.J., and Chikindas, M.L. (2011): Elucidation of the molecular mechanisms of action of the natural antimicrobial peptide subtilosin against the bacterial vaginosis-associated pathogen Gardnerella vaginalis. Probiotics & Antimicro. Prot., 3(1): 41? 47. doi:10.1007/s12602-010-9061-4.
- Nurudeen A. O., Chimezie P.O., and Folarin A. O. (2016): The Biotechnology of Ugba, a Nigerian Traditional Fermented Food Condiment. Front. Microbiol., 7: 115. doi:10.3389/fmicb.2016.01153.
- Odunfa, S., and Oyewole, O. (1986): Identification of Bacillus species from ?iru?, a fermented African locust bean product. J. Bas. Microbiol., 26(2): 101?108.
- Ogunshe, A. A.O., Ayodele A.E., and Okonko I.O. (2006): Microbial studies on aisa: a potential indigenous laboratory fermented food condiment from Albizia saman Jacq, F. Mull. Pakistan J. Nutrit., 5: 51?58.
- Ogunshe, A.A.O., Omotosho, M.O., and Ayansina A.D.V. (2007): Microbial studies and biochemical characteristics of controlled fermented Afiyo - a Nigeria fermented food condiment from Prosopis africana Guill and Perr. Taub. Pakistan J. Nutrit., 6: 620?627.
- Oguntoyinbo, F. A., Sanni, A.I., Franz, C.M.A.P., and Holzapfel, W.H. (2007): In vitro fermentation studies for selection and evaluation of Bacillus strains as starter cultures for the production of okpehe, a traditional African fermented condiment. Int. J. Food Microbiol.,113: 208?218.
- Oguntoyinbo, F.A, Huch, M., Cho, G.S., Schillinger, U., Holzapfel, W.H., Sanni, A.I., and Franz, C.M.A.P. (2010): Diversity of Bacillus species isolated from okpehe, a traditional fermented soup condiment from Nigeria. J. Food Protect., 73: 870?878.
- Okorie, P. C., and Olasupo, N. A. (2013a): Growth and extracellular enzyme production by microorganisms isolated from Ugba-an indigenous Nigerian fermented food. Afr. J. Biotechnol., 12: 4158?4167. doi: 10.5897/AJB11.2842.
- Omafuvbe, B. O., Falade, O. S., and Osuntogun, B.A. (2004): Chemical and biochemical changes in African Locust Bean Parkia biglobosa, and melon Citrullus vulgaris, seeds during Fermentation to condiments. Pakistan J. Nutrit., 3: 140 ?145.
- Omafuvbe, B.O., Shonukan, O.O., and Abiose, S.H. (2000): Microbiological and biochemical changes in the traditional fermentation of soybean for ?soy-dawadawa? - Nigerian food condiment. Food Microbiol.,17: 469?474.
- Ongena, M., Jacques, P. (2008): Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends in Microbiol., 16(3): 115?125.
- Osc?riz, J.C., Cintas, L., Holo, H., Lasa, I., Nes, I.F. and Pisabarro, A.G. (2006): Purification and sequencing of cerein 7B, a novel bacteriocin produced by Bacillus cereus Bc7. FEMS Microbiol. Lett., 254: 108?115.
- Ouoba, L.I.I, Parkouda, C., Diawara, B., Scotti, C., and Varnam, A. H.(2008a): Identification of Bacillus spp. from bikalga, fermented seeds of Hibiscus sabdariffa: phenotypic and genotypic characterization. J. Appl. Microbiol., 104: 122?131. doi: http://dx.doi.org/10.1111/j.1365-2672.2007.03550.
- Ouoba, L.I.I., Cantor, M.D., Diawara, B., Traore, A.S., and Jakobsen, M. (2003b): Degradation of African Locust Bean oil by Bacillus subtilis and Bacillus pumilus isolated from soumbala, a fermented African Locust Bean condiment. J. Appl. Microbiol., 95: 868?873.
- Ouoba, L.I.I., Diawara, B., Annan, N.T., Poll, L., and Jakobsen, M. (2005): Volatile compounds of Soumbala, a fermented African locust bean Parkia biglobosa, food condiment. J. Appl. Microbiol., 99: 1413?1421.
- Ouoba, L.I.I., Diawara, B., Christensen, T., Mikkelsen, J.D., and Jakobsen, M. (2007a): Degradation of polysaccharides and non-digestible oligosaccharides by Bacillus subtilis and Bacillus pumilus isolated from soumbala, a fermented African locust bean Parkia biglobosa, food Condiment. Euro. Food Res. & Technol., 224: 689?694.
- Ouoba, L.I.I., Diawara, B., Jespersen, L., and Jakobsen, M. (2007b): Antimicrobial activity of Bacillus subtilis and Bacillus pumilus during the fermentation of African locust bean Parkia biglobosa, for soumbala production. J. Appl. Microbiol.,102: 963?970.
- Ouoba, L.I.I., Rechinger, K.B., Barkholt, V., Diawara, B., Traore, A.S., and Jakobsen, M. (2003a): Degradation of proteins during the fermentation of African Locust Bean Parkia biglobosa, by strains of Bacillus subtilis and Bacillus pumilus for production of soumbala. J. Appl. Microbiol., 94: 396?402.
- Ouoba, L.L.I., Diawara, B., moa-Awua, W.K., Traor?, A.S., and Moller, P.L. (2004): Genotyping of starter cultures of Bacillus subtilis and Bacillus pumilus for fermentation of African locust bean Parkia biglobosa, to produce soumbala. Int. J. Food Microbiol., 90: 197?205.
- Paik S. H., Chakicherla A., and Hansan J.H. (1998): Identification and characterization of the structural and transporter genes for, and the chemical and biological properties of, Sublancin 168, a novel lantibiotic produced by Bacillus subtilis 168. J. Biol. Chem., 273(36): 23134-23142. doi.10.1074/jbc.273.36.23134.
- P?lffy R., Gardl?k R., Behuliak M., Kadasi L., Turna J., and Celec, P. (2009): On the physiology and pathophysiology of antimicrobial peptides. Mol. Med., 15(1-2): 51?59. doi:10.2119/molmed.2008.00087.
- Parisot, J., Carey, S., Breukink, E., Chan, W.C., Narbad, A., Bonev, B. (2008): Molecular mechanism of target recognition by subtilin, a class I lanthionine antibiotic. Antimicrobial Agents and Chemotherapy., 52: 612?618.
- Parkouda, C., Nielsen, D.S., Azokpota, P., Ouoba, L.I.I., Amoa-Awua, W.K., Thorsen, L., Hounhouigan, J.D., Jensen, J.H., Tano-Debrah, K., Diawara, B. and Jakobsen, M. (2009): The microbiology of alkaline-fermentation of indigenous seeds used as food condiments in Africa and Asia. Cr. Rev. Microbiol., 35(1): 139?156.
- Parkouda, C., Thorsen, L., Compaor?, C.S., Nielsen, D.S., Tano-Debrah, K., Jensen, J.S., Diawara, B., Jakobsen, M., (2010): Microorganisms associated with maari, a Baobab seed fermented product. Int. J. Food Microbiol., 142: 292?301.
- Pathak, K.V., Keharia, H., Gupta, K., Thakur, S. S., and Balaram, P. (2012): Lipopeptides from the banyan endophyte, Bacillus subtilis K1: mass spectrometric characterization of a library of fengycins. J. American Soci. Mass Spec., 23(10): 1716?1728.
- Pattnaik, P., Grover, S., and Batish, V.K. (2005): Effect of environmental factors on production of lichenin, a chromosomally encoded bacteriocin-like compound produced by Bacillus licheniformis 26L-10/3RA. Microbiol. Res., 160: 213?218.
- Peypoux, F., Bonmatin, J.M., and Wallach, J. (1999): Recent trends in the biochemistry of surfactin. Appl. Microbiol. Biotechnol. 51(5): 553?563. doi :10.1007/s002530051432.
- Peypoux, F., Pommier, M.T., Marion, D., Ptak, M., Das, B.C., and Michel, G. (1986): Revised structure of mycosubtilin, a peptidolipid antibiotic from Bacillus subtilis. J. Antibiot., 39(5): 636?641.
- Ross R.P., Morgan S., and Hill, C. (2002): Preservation and fermentation: past, present and future. Int. J. Food Microbiol., 79(1): 3?16. doi: http://dx.doi.org/10.1016/S0168-1605(02) 00174-5.
- Sanni, A. I, Onilude, A. A, Fadahunsi, I.F., Ogunbanwo, S.T., and Afolabi, R.O. (2002): Selection of starter cultures for the production of ugba, a fermented soup condiment. Euro. Food Res. & Technol., 215: 176?180
- Sanni, A. I., Ayernor, G.S., Sakyi-Dawson, E., and Sefa-Dedeh, S. (2000): Aerobic spore-forming bacteria and chemical composition of some Nigerian fermented soup condiments. Plant Foods for Human Nutrit., 55: 111?118.
- Sanni, A. I., and Ogbonna, D.N. (1991): The production of owoh - A Nigerian fermented seasoning agent from cotton seed Gossypium Hirsutum L. Food Microbiol., 8: 223?229.
- Sarkar, P. K., Hasenack, B., and Nout M. J. R. (2002): Diversity and functionality of Bacillus and related genera isolated from spontaneously fermented soybeans Indian kinema, and locust beans African soumbala. Int. J. Food Microbiol., 77: 175?86.
- Savadogo, A., Tapi, A., Chollet, M., Wathelet, B., Traor?, A.S., Jacques, P. (2011): Identification of surfactin producing strains in Soumbala and Bikalga fermented condiments using polymerase chain reaction and matrix assisted laser desorption/ ionization-mass spectrometry methods. Int. J. Food Microbiol., 151: 299?306.
- Schwarzer, D., Finking, R., and Marahiel, M.A. (2003): Non-ribosomal peptides: from genes to products. Nat. Product Rep., 20(3): 275?287. doi: http://dx.doi.org/10.1002/chin.200338264.
- Sebei, S., Zendo, T., Boudabous, A., Nakayama, J., and Sonomoto, K. (2007): Characterization, N-terminal sequencing and classification of cerein MRX1, a novel bacteriocin purified from a newly isolated bacterium: Bacillus cereus MRX1. J. Appl. Microbiol., 103: 1621?1631.
- Serizawa, M., Kodama, K., Yamamoto, H., Kobayashi, K., Ogasawara, N., and Sekiguchi, J. (2005): Functional analysis of the YvrGHb two-component system of Bacillus subtilis: identification of the regulated genes by DNA microarray and Northern blot analyses. Biosci. Biotech. Bioch., 69: 2155?2169.
- Svetoch, E.A., Stern, N.J., Eruslanov, B.V. et al. (2005): Isolation of Bacillus circulans and Paenibacillus polymyxa strains inhibitory to Campylobacter jejuni and characterization of associated bacteriocins. J. Food Protect., 68: 11?17.
- Seydlov?, G., Cabala, R., and Svobodov?, J. (2011): Biomedical engineering, trends, research and technologies, in Surfactin-Novel Solutions for Global Issues. In Tech, Rijeka, Croatia.,13: 306?330.
- Sieber, S.A., and Marahiel, M.A. (2005): Molecular mechanisms underlying non-ribosomal peptide synthesis: approaches to new antibiotics. Chem. Rev., 105(2): 715?738. doi: http://dx.doi.org/10.1021/cr0301191.
- Siezen, R.J., Kuipers, O.P., and de Von W.M. (1996): Comparison of lantibiotic gene clusters and encoded proteins. Antonie Van Leeuwenhoek., 69: 171?184.
- Silva, C.C.G., Silva, S.P.M., and Ribeiro S.C. (2018): Application of Bacteriocins and Protective Cultures in Dairy Food Preservation. Front. Microbiol., 9:594. doi: 10.3389/fmicb.2018.00594.
- Simha B.V., Sood, S., Kumariya, R., and Garsa, A.K. (2012): Simple and rapid purification of pediocin PA-1 from Pediococcus pentosaceous NCDC 273 suitable for industrial application. Microbiol. Res., 167: 544?549. doi: 10.1016/j.micres.2012.01.001.
- Slepecky, R.A., and Hemphill, H.E. (2006): What is a Bacillus? In: Doi, R.H., McGloghlin, M. Biology of Bacilli: Applications to industry. Butterworth-Heinemann, Boston, MA, pp.1?21.
- Stein T., D?sterhus, S., Stroh, A., Entian, K.D. (2004): Subtilosin production by two Bacillus subtilis subspecies and variance of the sbo-alb cluster. Appl. Environ. Microbiol., 70: 2349?2353. [PubMed: 15066831].
- Stein, T. (2005): Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol., 56(4): 845?857. doi:10.1111/j.1365-2958.2005.04587.
- Stein, T. (2008): Whole-cell matrix-assisted laser desorption/ionization mass spectrometry for rapid identification of bacteriocin/lantibiotic-producing bacteria. Rap. Commun. Mass Sp., 22: 1146?1152.
- Stein, T., Borchert, S., Conrad, B., Feesche, J., Hofemeister, B., Hofemeister, J., and Entian, K.D. (2002a): Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3. J. Bacteriol., 184: 1703?1711.
- Stein, T., Heinzmann, S., Kiesau, P., Himmel, B., and Entian, K.D. (2003): The spa box for transcriptional activation of subtilin biosynthesis and immunity in Bacillus subtilis. Mol. Microbiol., 47: 1627?1636.
- Steller, S. et al. (2004): Initiation of surfactin biosynthesis and the role of the SrfD-thioesterase protein. Biochem., 43: 11331?11343.
- Strieker, M., Tanović, A., and Marahiel, M.A. (2010): Non-ribosomal peptide synthetases: structures and dynamics. Curr. Op. Struct. Biol., 20(2): 234?240. doi: http://dx.doi.org/10.1016/j.sbi.2010.01.009.
- Sutyak, K. E., Wirawan, R.E., Aroutcheva, A.A., and Chikindas, M.L. (2008b): Isolation of the Bacillus subtilis antimicrobial peptide subtilosin from the dairy product-derived Bacillus amyloliquefaciens. J. Appl. Microbiol., 104(4): 1067?1074. doi:10.1111/j.1365-2672.2007.03626.
- Taal?, E., Savadogo, A., Zongo, C., Somda, M. K., Sereme, S.S., Karou, S.D., Soulama, I., and Traor?, A.S. (2015). Characterization of Bacillus species producing Bacteriocin-like inhibitory substances (BLIS) isolated from fermented food in Burkina Faso. Int. J. Adv. Res. Biol. Sci. 2(4): 279?290.
- Tambadou, F. (2014) : ?tude de la production de peptides non-ribosomiques chez des souches de Paenibacillus. PhD Thesis, Universit? de La Rochelle, La Rochelle, 222p.
- Tapi, A., Chollet-Imbert, M., Scherens, B., and Jacques, P. (2010): New approach for the detection of non-ribosomal peptide synthetase genes in Bacillus strains by polymerase chain reaction. Appl. Microbiol. Biotech., 85: 1521?1531.
- Terlabie, N.N., Sakyi-Dawson, E., Amoa-Awua, W.K., Terlabie, N.N., and Sakyi-Dawson, E., (2006): The comparative ability of four isolates of Bacillus subtilis to ferment soybeans into dawadawa. Int. J. Food Microbiol.,106: 145?152.
- Wang, J., Liu, J., Wang, X., Yao, J., and Yu, Z. (2004): Application of electrospray ionization mass spectrometry in rapid typing of fengycin homologues produced by Bacillus subtilis. Lett. Appl. Microbiol., 39: 98?102.
- Wang, J., and Fung, D.Y.C. (1996): Alkaline-fermented foods: A review with emphasis on pidan fermentation. Crit. Rev. Microbiol., 22: 101?138.
- Zhang, B., Dong, C., Shang, Q., Han, Y., and Li, P. (2013): New insights into membrane-active action in plasma membrane of fungal hyphae by the lipopeptide antibiotic bacillomycin L. Biochim. Biophy. Acta.,1828(9): 2230?2237.doi: 10.1016/j.bbamem.201305.033.
- Zheng, G., and Slavik, M.F. (1999): Isolation, partial purification and characterization of a bacteriocin produced by a newly isolated Bacillus subtilis strain. Lett. Appl. Microbiol., 28(5): 363?367. doi:10.1046/j.1365-2672.1999.00545.
- Zheng, G., Hehn, R., and Zuber, P. (2000): Mutational analysis of the sbo-alb locus of Bacillus subtilis: identification of genes required for subtilosin production and immunity. J. Bacteriol., 182: 3266?3273.
- Zou, A., Liu, J., Garamus, V.M., Yang, Y., Willumeit, R., and Mu, B. (2010). Micellization activity of the natural lipopeptide [Glu1, Asp5] Surfactin-C15 in aqueous solution. J. Phys. Chem.,114(8): 2712?2718.
[Yerobessor Dabire, Marius K. Somda, Jerry Ugwuanyi, Lewis I. Ezeogu and Alfred S. Traore. (2018); DIVERSITY OF BACILLUS SPECIES AND THEIR ANTIMICROBIAL COMPOUNDS INVOLVED IN ALKALINE-FERMENTATION OF INDIGENOUS FOOD CONDIMENTS USED IN AFRICA. Int. J. of Adv. Res. 6 (Dec). 331-355] (ISSN 2320-5407). www.journalijar.com
Biochemistry-Microbiology