Bacillus amyloliquefaciens ssp. plantarum strains as potential protective starter cultures for the production of Bikalga, an alkaline fermented food

Journal of Applied Microbiology

Volumn 115, Issue 1, 2013, Pages 133-146

  Compaore C S ^a,b,c   Nielsen, D S ^b   Sawadogo Lingani, H ^a   Berner, T S ^b   Nielsen, K F ^d   Adimpong, D B ^b   Diawara, B ^a   Ouedraogo G A ^c   Jakobsen, M ^b   Thorsen, L ^b  

^a Centre National de la Recherche Scientifique Ouagadougou   (Burkina Faso)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Polytechnic University of Bobo Dioulasso   (Burkina Faso)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Antimicrobial activity; Bacillus amyloliquefaciens ssp. plantarum; Bikalga; Lipopeptides; Polyketides; Starter cultures

Indexed keywords

BACTERIOLOGY; BRAIN; FOOD PROCESSING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY;

ANTI-MICROBIAL ACTIVITY; BACILLUS AMYLOLIQUEFACIEN SSP.; BACILLUS AMYLOLIQUEFACIENS; BIKALGA; BRAIN HEART INFUSIONS; H. SABDARIFFA; LIPOPEPTIDES; PLANTARUM; POLYKETIDES; STARTER CULTURES;

BACILLUS CEREUS;

BACILLAENE; BACILYSIN; DIFFICIDIN; DNA TOPOISOMERASE (ATP HYDROLYSING) B; FENGYCIN; ITURIN A; MACROLACTIN; SURFACTIN; UNCLASSIFIED DRUG;

AGAR; ALKALINITY; ANTIBIOTICS; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOLOGICAL CONTROL; BRAIN; FERMENTATION; FOOD; GENE EXPRESSION; MASS SPECTROMETRY; PATHOGEN;

ALKALINITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACILLUS CEREUS; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; FERMENTED PRODUCT; GENE SEQUENCE; HIBISCUS SABDARIFFA; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PHENOTYPE; PLANT SEED; POLYMERASE CHAIN REACTION; TIME OF FLIGHT MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY;

BACILLUS AMYLOLIQUEFACIENS; BACILLUS CEREUS; FUNGI; HIBISCUS SABDARIFFA; NEGIBACTERIA; POSIBACTERIA;

EID: 84879109416     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12214     Document Type: Article

References (50)

1. Abriouel, H., Franz, C.M.A.P., Omar, N.B. and Gálvez, A. (2010) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35, 201-232.
2. Agata, N., Mori, M., Ohta, M., Suwan, S., Ohtani, I. and Isobe, M. (1994) A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in HEp-2 cells. FEMS Microbiol Lett 121, 31-34.
3. Agbobatinkpo, P.B., Thorsen, L., Nielsen, D.S., Azokpota, P., Akissoe, N., Hounhouigan, J.D. and Jakobsen, M. (2013) Biodiversity of aerobic Endospore-Forming Bacterial species occurring in Yanyanku and Ikpiru, fermented seeds of Hibiscus sabdariffa used to produce food condiments in Benin. Int J Food Microbiol 163, 231-238.
4. Bengaly, M.D., Béré, A. and Traoré, A. (2006) The chemical composition of bikalga, a traditional fermented roselle (Hibiscus sabdariffa L.) seeds condiment. Part II: evaluation of mineral, total polyphenols and phytic acid content, predicting the iron bioavailability. Elec J Food Plant Chem 1, 7-11.
5. Benitez, L.B., Velho, V.R., Lisboa, P.M., da Costa Medina, F.L. and Brandelli, A. (2010) Isolation and characterization of antifungal peptides produced by Bacillus amyloliquefaciens LBM5006. J Microbiol 48, 7791-7797.
6. Benitez, L.B., Caumo, K., Brandelli, A. and Rott, B.M. (2011) Bacteriocin-like substance from Bacillus amyloliquefaciens shows remarkable inhibition of Acanthamoeba polyphaga. Parasitol Res 108, 687-691.
7. Bizani, D. and Brandelli, A. (2002) Characterization of a bacteriocin produced by a newly isolated Bacillus sp. strain 8A. J Appl Microbiol 93, 512-519.
8. Borriss, R., Chen, X.-H., Rückert, C., Blom, J., Becker, A., Baumgarth, B., Fan, B., Pukall, R. et al. (2011) Relationship of Bacillus amyloliquefaciens clades associated with strains DSM 7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons. Int J Syst Evol Microbiol 61, 1786-1801.
9. Butcher, R.A., Schroeder, F.C., Fischbach, M.A., Straight, P.D., Kolter, R., Walsh, C.T. and Clardy, J. (2007) The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc Natl Acad Sci USA 104, 1506-1509.
10. Cao, X.-H., Liao, Z.-Y., Wang, C.-L., Yang, W.-Y. and Lu, M.-F. (2009) Evaluation of a lipopeptide biosurfactant from Bacillus natto tk-1 as a potential source of anti-adhesive, antimicrobial and antitumor activities. Braz J Microbiol 40, 373-379.
11. Chen, X.H., Koumoutsi, A., Scholz, R., Schneider, K., Vater, J., Süssmuth, R., Piel, J. and Borriss, R. (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140, 27-37.
12. Chung, S., Kong, H., Buyer, J.S., Lakshman, D.K., Lydon, J., Kim, S.-D. and Roberts, D.P. (2008) Isolation and partial characterization of Bacillus subtilis ME488 for suppression of soilborne pathogens of cucumber and pepper. Appl Microbiol Biotechnol 80, 115-123.
13. Guo, Y., Huang, E., Yuan, C., Zhang, L. and Yousef, A.E. (2012) Isolation of a Paenibacillus sp. strain and structural elucidation of its broad-spectrum lipopeptide antibiotic. Appl Environ Microbiol 78, 3156.
14. Halimi, B., Dortu, C., Arguelles-Arias, A., Thonart, P., Joris, B. and Fickers, P. (2010) Antilisterial activity on poultry meat of amylolysin, a bacteriocin from Bacillus amyloliquefaciens GA1. Probiotics Antimicro Prot 2, 120-125.
15. Holzapfel, W.H. (2002) Appropriate starter culture technologies for small-scale fermentation in developing countries. Int J Food Microbiol 75, 197-212.
16. Huang, X., Lu, Z., Bie, X., Lu, F., Zhao, H. and Yang, S. (2007) Optimization of inactivation of endospores of Bacillus cereus by antimicrobial lipopeptides from Bacillus subtilis fmbj strains using a response surface method. Appl Microbiol Biotechnol 74, 454-461.
17. Huang, X., Gao, X., Zheng, L. and Hao, G. (2009) Optimization of sterilization of Salmonella enteritidis in meat by surfactin and iturin using a response surface method. Int J Pept Res Ther 15, 61-67.
18. Kaboré, D., Thorsen, L., Nielsen, S.D., Berner, S.T., Sawadogo-Lingani, H., Diawara, B., Dicko, H.M. and Jakobsen, M. (2012) Bacteriocin formation by dominant aerobic sporeformers isolated from traditional maari. Int J Food Microbiol 154, 10-18.
19. Koumoutsi, A., Chen, X.H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., Vater, J. and Borriss, R. (2004) Structural and functional characterization of gene clusters directing non-ribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186, 1084-1096.
20. Lindegaard Pedersen, L., Owusu-Kwarteng, J., Thorsen, L. and Jespersen, L. (2012) Biodiversity and probiotic potential of yeasts isolated from Fura, a West African spontaneously fermented cereal. Int J Food Microbiol 159, 144-151.
21. Lisboa, M.P., Bonatto, D., Bizani, D., Henriques, J.A.P. and Brandelli, A. (2006) Characterization of a bacteriocin-like substance produced by Bacillus amyloliquefaciens isolated from the Brazilian Atlantic forest. Int Microbiol 9, 111-118.
22. Lund, T., De Buyser, M.L. and Granum, P.E. (2000) A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol Microbiol 38, 254-261.
23. Madhaiyan, M., Poonguzhali, S., Kwon, S.W. and Sa, T.M. (2010) Bacillus methylotrophicus sp. nov., a methanol-utilizing, plant-growth-promoting bacterium isolated from rice rhizosphere soil. Int J Syst Evol Microbiol 60, 2490-2495.
24. Maget-Dana, R., Thimon, L., Peypoux, F. and Ptak, M. (1992) Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74, 1047-1051.
25. Motta, A.S., Lorenzini, D.M. and Brandelli, A. (2007a) Purification and partial characterization of an antimicrobial peptide produced by a novel Bacillus sp. isolated from the Amaon Basin. Curr Microbiol 54, 282-286.
26. Motta, A.S., Cannavan, F.S., Tsai, S. and Brandelli, A. (2007b) Characterization of a broad range antibacterial substance from a new Bacillus species isolated from Amazon basin. Arch Microbiol 188, 367-375.
27. Nielsen, K.F., Månsson, M., Rank, C., Frisvad, J.C. and Larsen, T.O. (2011) Dereplication of microbial natural products by LC-DAD-TOFMS. J Nat Prod 74, 2338-2348.
28. Ongena, M. and Jacques, P. (2008) Bacillus lipopeptides: versatile weapons for plant disease control. Trends Microbiol 16, 115-125.
29. Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J.L. and Thonart, P. (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9, 1084-1090.
30. Ouoba, L.I.I., Diawara, B., Jespersen, L. and Jakobsen, M. (2007) 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.
31. 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.
32. Ouoba, L.I.I., Thorsen, L. and Varnam, A.H. (2008b) Enterotoxins and emetic toxins production by Bacillus cereus and other species of Bacillus isolated from Soumbala and Bikalga, African alkaline fermented food condiments. Int J Food Microbiol 124, 224-230.
33. Paik, S.H., Chakicherla, A. and Hansen, J.N. (1998) Identification and characterization of 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, 134-142.
34. Patel, P.S., Hang, S., Fisher, S., Pirnik, D., Aklonis, C., Dean, L., Meyers, E., Fernandes, P. et al. (1995) Bacillaene, a novel inhibitor of procaryotic protein synthesis produced by Bacillus sbtilis: production, taxonomy, isolation, physisco-chemical characterization and biological activity. J Antibiot 48, 997-1003.
35. Romero, D., De Vicente, A., Rakotoaly, R.H., Dufour, S.E., Veening, J.W., Arrebola, E., Cazorla, F.M., Kuipers, O.P. et al. (2007) The iturin and fungycin families of lipopeptides are keys factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Pathogen Interact 20, 430-440.
36. Rückert, C., Blom, J., Chen, X.-H., Reva, O. and Borriss, R. (2011) Genome sequence of B. amyloliquefaciens type strain DSM7T reveals differences to plant-associated B. amyloliquefaciens FZB42. J Biotechnol 155, 78-85.
37. Sarangi, N.P., Athukorala, W.G., Dilantha, F. and Khalid, Y.R. (2009) Identification of antifungal antibiotics of Bacillus species isolated from different microhabitats using polymerase chain reaction and MALDI-TOF mass spectrometry. Can J Microbiol 55, 1021-1032.
38. Savadogo, A., Tapi, A., Chollet, M., Wathelet, B., Traoré, A.S. and 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.
39. Stein, T. (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56, 845-857.
40. Stein, T., Borchert, S., Conrad, B., Feesche, J., Hofemeister, B., Hofemeister, J. and Entian, K.D. (2002) Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A l/3. J Bacteriol 184, 1703-1711.
41. Stenfors, L.P. and Granum, P.E. (2001) Psychrotolerant species from the Bacillus cereus group are not necessarily Bacillus weihenstephanensis. (FEMS) Microbiol Lett 197, 223-228.
42. Sutyak, K.E., Wirawan, R.E., Aroutcheva, A.A. and Chikindas, M.L. (2008) Isolation of the Bacillus subtilis antimicrobial peptide subtilosin from the dairy product-derived Bacillus amyloliquefaciens. J Appl Microbiol 104, 1067-1074.
43. Tabbene, O., Slimene, B.I., Djebali, K., Mangoni, A.-L., Urdaci, M.-C. and Limam, F. (2009) Optimization of medium composition for the production of antimicrobial activity by Bacillus subtilis B38. Biotechnol Prog 25, 1267-1274.
44. 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 Biotechnol 85, 1521-1531.
45. Thorsen, L., Azokpota, P., Hansen, B.M., Hounhouigan, D.J. and Jakobsen, M. (2010) Identification, genetic diversity and cereulide producing ability of Bacillus cereus group strains isolated from Beninese traditional fermented food condiments. Int J Food Microbiol 142, 247-250.
46. Tosato, V., Albertini, A.M., Zotti, M., Sonda, S. and Bruschi, C.V. (1997) Sequence completion, identification and definition of the fengycin operon in Bacillus subtilis 168. Microbiology 143, 3443-3450.
47. Tsuge, K., Akiyama, T. and Shoda, M. (2001) Cloning, sequencing, and characterization of the iturin A operon. J Bacteriol 183, 6265-6273.
48. Wang, L.T., Lee, F.L., Tai, C.J. and Kasai, H. (2007) Comparison of gyrB gene sequences, 16S rRNA gene sequences and DNA-DNA hybridization in the Bacillus subtilis group. Inter J Syst Evol Microbiol 57, 1846-1850.
49. Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S. and Madden, T. (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134.
50. Zimmerman, S.B., Schwartz, C.D., Monaghan, R.L., Pelak, B.A., Weissberger, B., Gilfillan, E.C., Mochales, S., Hernandez, S. et al. (1986) Difficidin and oxydifficidin: novel broad spectrum antibacterial antibiotics produced by Bacillus Subtilis. I. Production. Taxonomy and antibacterial activity. J Antibiot 12, 1677-1681.