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First Insight into the Technological Features of Lactic Acid Bacteria Isolated from Algerian Fermented Wheat Lemzeiet

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Abstract

Fermented cereals are part of the main traditional diets of many people in Africa, usually obtained from artisanal production. The intensification of their manufacturing, responding to the consumers demand, requires a better control to ensure their sanitary, nutritional, and taste qualities, hence, the need of selecting accurate and safe starter cultures. In the present study, 48 lactic acid bacteria (LAB) strains, previously isolated from Algerian fermented wheat lemzeiet, were analyzed for different technological properties. 14 LAB strains, belonging to Pediococcus pentosaceus, Enterococcus faecium, Lactobacillus curvatus, Lactobacillus brevis, and Leuconostoc mesenteroides species, decreased rapidly the pH of the flour extract broth close to 4 or below. 91% of strains showed extracellular protease activity, but only 12% were amylolytics. 18 LAB strains inhibited or postponed the growth of three fungal targets Rhodotorula mucilaginosa UBOCC-A-216004, Penicillium verrucosum UBOCC-A-109221, and Aspergillus flavus UBOCC-A-106028. The strains belonging to Lactobacillus spp., Leuconostoc fallax, L. mesenteroides, and Weissella paramesenteroides were the most antifungal ones. Multiplex PCR for biogenic amines’ production did not reveal any of the genes involved in the production of putrescine, histamine, and tyramine for 17 of the 48 strains. The obtained results provided several candidates for use as starter culture in the future production of lemzeiet.

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References

  1. Bourdichon F, Casaregola S, Farrokh C et al (2012) Food fermentations: microorganisms with technological beneficial use. Int J Food Microbiol 154:87–97. https://doi.org/10.1016/j.ijfoodmicro.2011.12.030

    Article  CAS  PubMed  Google Scholar 

  2. Ferri M, Serrazanetti DI, Tassoni A et al (2016) Improving the functional and sensorial profile of cereal-based fermented foods by selecting Lactobacillus plantarum strains via a metabolomics approach. Food Res Int 89:1095–1105. https://doi.org/10.1016/j.foodres.2016.08.044

    Article  CAS  Google Scholar 

  3. Franz CMAP, Holzapfel W (2011) The importance of understanding the stress physiology of lactic acid bacteria. In: Tsakalidou E, Papadimitriou K (eds) Stress responses of lactic acid bacteria. Springer, New York, p 530

    Google Scholar 

  4. Salminen S, von Wright A, Ouwehand A (2005) Lactic acid bacteria, microbiological and functional aspects third edition, revised and expanded. Marcel Dekker, New York

    Google Scholar 

  5. Guyot JP (2012) Cereal-based fermented foods in developing countries: ancient foods for modern research. Int J Food Sci Technol 47:1109–1114. https://doi.org/10.1111/j.1365-2621.2012.02969.x

    Article  CAS  Google Scholar 

  6. Franz CMAP, Huch M, Mathara JM et al (2014) African fermented foods and probiotics. Int J Food Microbiol 190:84–96. https://doi.org/10.1016/j.ijfoodmicro.2014.08.033

    Article  CAS  PubMed  Google Scholar 

  7. Holzapfel WH (2002) Appropriate starter culture technologies for small-scale fermentation in developing countries. Small-Scale Ferment Dev Ctries 75:197–212. https://doi.org/10.1016/S0168-1605(01)00707-3

    Article  CAS  Google Scholar 

  8. Tamang JP (2010) Diversity of fermented foods. In: In: Tamang JP, Kailasapathy K (eds) Fermented foods and beverages of the world. CRC Press/Taylor & Francis, Boca Raton, p 448

    Chapter  Google Scholar 

  9. Akabanda F, Owusu-Kwarteng J, Tano-Debrah K et al (2014) The use of lactic acid bacteria starter culture in the production of Nunu, a spontaneously fermented milk product in Ghana. Int J Food Sci 2014:1–11. https://doi.org/10.1155/2014/721067

    Article  Google Scholar 

  10. Guyot JP (2010) Fermented cereal products. In: Tamang JP, Kailasapathy K (eds) Fermented foods and beverages of the world. CRC Press/Taylor & Francis, Boca Raton p 448

    Google Scholar 

  11. Ogunremi OR, Banwo K, Sanni AI (2017) Starter-culture to improve the quality of cereal-based fermented foods: trends in selection and application. Curr Opin Food Sci 13:38–43. https://doi.org/10.1016/j.cofs.2017.02.003

    Article  Google Scholar 

  12. Ruiz Rodríguez L, Vera Pingitore E, Rollan G et al (2016) Biodiversity and technological-functional potential of lactic acid bacteria isolated from spontaneously fermented quinoa sourdoughs. J Appl Microbiol 120:1289–1301. https://doi.org/10.1111/jam.13104

    Article  CAS  PubMed  Google Scholar 

  13. Salvucci E, LeBlanc JG, Pérez G (2016) Technological properties of Lactic acid bacteria isolated from raw cereal material. LWT - Food Sci Technol 70:185–191. https://doi.org/10.1016/j.lwt.2016.02.043

    Article  CAS  Google Scholar 

  14. Settanni L, Ventimiglia G, Alfonzo A et al (2013) An integrated technological approach to the selection of lactic acid bacteria of flour origin for sourdough production. Food Res Int 54:1569–1578. https://doi.org/10.1016/j.foodres.2013.10.017

    Article  CAS  Google Scholar 

  15. Shalaby AR (1996) Significance of biogenic amines to food safety and human health. Food Res Int 29:675–690. https://doi.org/10.1016/S0963-9969(96)00066-X

    Article  CAS  Google Scholar 

  16. Bekhouche F, Merabti R, Bailly JD (2013) Traditional couscous manufacture from fermented wheat (Algeria) investigation of the process and estimation of the technological and nutritional quality. Afr J Food Sci Technol 4:167–175. https://doi.org/10.14303/ajfst.2013.032

    Article  Google Scholar 

  17. Merabti R, Bekhouche F, Chuat V et al (2015) A large diversity of lactic acid bacteria species is involved in the fermentation of wheat used for the manufacture of lemzeiet. Eur Food Res Technol 241:137–149. https://doi.org/10.1007/s00217-015-2442-x

    Article  CAS  Google Scholar 

  18. Coton M, Romano A, Spano G et al (2010) Occurrence of biogenic amine-forming lactic acid bacteria in wine and cider. Food Microbiol 27:1078–1085. https://doi.org/10.1016/j.fm.2010.07.012

    Article  CAS  PubMed  Google Scholar 

  19. Thierry A, Valence F, Deutsch S-M et al (2015) Strain-to-strain differences within lactic and propionic acid bacteria species strongly impact the properties of cheese–a review. Dairy Sci Technol 95:895–918. https://doi.org/10.1007/s13594-015-0267-9

    Article  CAS  Google Scholar 

  20. Alfonzo A, Ventimiglia G, Corona O et al (2013) Diversity and technological potential of lactic acid bacteria of wheat flours. Food Microbiol 36:343–354. https://doi.org/10.1016/j.fm.2013.07.003

    Article  CAS  PubMed  Google Scholar 

  21. Herranen M, Kariluoto S, Edelmann M et al (2010) Isolation and characterization of folate-producing bacteria from oat bran and rye flakes. Int J Food Microbiol 142:277–285. https://doi.org/10.1016/j.ijfoodmicro.2010.07.002

    Article  CAS  PubMed  Google Scholar 

  22. Kouker G, Jaeger KE (1987) Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol 53:211–213

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Le Lay C, Mounier J, Vasseur V et al (2016) In vitro and in situ screening of lactic acid bacteria and propionibacteria antifungal activities against bakery product spoilage molds. Food Control 60:247–255. https://doi.org/10.1016/j.foodcont.2015.07.034

    Article  CAS  Google Scholar 

  24. Parayre S, Falentin H, Madec MN et al (2007) Easy DNA extraction method and optimisation of PCR-temporal temperature gel electrophoresis to identify the predominant high and low GC-content bacteria from dairy products. J Microbiol Methods 69:431–441. https://doi.org/10.1016/j.mimet.2007.02.011

    Article  CAS  PubMed  Google Scholar 

  25. Corsetti A, Perpetuini G, Tofalo R (2015) Biopreservation effects in fermented foods. In: Holzapfel W (ed) Advances in fermented foods and beverages. Woodhead Publishing, Boston, pp 311–332

    Chapter  Google Scholar 

  26. Dalié DKD, Deschamps AM, Richard-Forget F (2010) Lactic acid bacteria—potential for control of mould growth and mycotoxins: a review. Food Control 21:370–380. https://doi.org/10.1016/j.foodcont.2009.07.011

    Article  CAS  Google Scholar 

  27. Kamal-Eldin A (2012) The role of fermentation in providing biologically active compounds for the human organism. In: Mehta BM, Kamal-Eldin A, Iwanski RZ (eds) Fermentation: effects on food properties. CRC Press, Boca Raton

    Google Scholar 

  28. Oliveira PM, Zannini E, Arendt EK (2014) Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: from crop farming to cereal products. Food Microbiol 37:78–95. https://doi.org/10.1016/j.fm.2013.06.003

    Article  CAS  PubMed  Google Scholar 

  29. Gänzle M, Loponen J, Gobbetti M (2008) Proteolysis in sourdough fermentations: mechanisms and potential for improved bread quality. Trends Food Sci Technol 19:513–521. https://doi.org/10.1016/j.tifs.2008.04.002

    Article  CAS  Google Scholar 

  30. Brandt MJ (2015) Quality improvement and fermentation control in dough fermentations. In: Advances in fermented foods and beverages: improving quality, technologies and health benefits, 1st edn. Woodhead Publishing, Boston

  31. Sanni AI, Morlon-Guyot J, Guyot JP (2002) New efficient amylase-producing strains of Lactobacillus plantarum and L. fermentum isolated from different Nigerian traditional fermented foods. Int J Food Microbiol 72:53–62. https://doi.org/10.1016/S0168-1605(01)00607-9

    Article  CAS  PubMed  Google Scholar 

  32. Songré-Ouattara LT, Mouquet-Rivier C, Icard-Vernière C et al (2008) Enzyme activities of lactic acid bacteria from a pearl millet fermented gruel (ben-saalga) of functional interest in nutrition. Int J Food Microbiol 128:395–400. https://doi.org/10.1016/j.ijfoodmicro.2008.09.004

    Article  CAS  PubMed  Google Scholar 

  33. Endo A, Dicks LMT (2014) Physiology of the LAB. In: Holzapfel WH, Wood BJB (eds) Lactic acid bacteria: biodiversity and taxonomy. Wiley Online Library, p 13

  34. Gänzle M, Follador R (2012) Metabolism of oligosaccharides and starch in lactobacilli: a review. Front Microbiol 3:340. https://doi.org/10.3389/fmicb.2012.00340

    Article  PubMed  PubMed Central  Google Scholar 

  35. Shibata K, Flores DM, Kobayashi G, Sonomoto K (2007) Direct l-lactic acid fermentation with sago starch by a novel amylolytic lactic acid bacterium, Enterococcus faecium. Enzyme Microb Technol 41:149–155. https://doi.org/10.1016/j.enzmictec.2006.12.020

    Article  CAS  Google Scholar 

  36. Unban K, Kanpiengjai A, Takata G et al (2017) Amylolytic enzymes acquired from L-Lactic acid producing Enterococcus faecium K-1 and improvement of direct lactic acid production from cassava starch. Appl Biochem Biotechnol 183:155–170. https://doi.org/10.1007/s12010-017-2436-1

    Article  CAS  PubMed  Google Scholar 

  37. Haydersah J, Chevallier I, Rochette I et al (2012) Fermentation by amylolytic lactic acid bacteria and consequences for starch digestibility of plantain, breadfruit, and sweet potato flours. J Food Sci 77:M466–M472. https://doi.org/10.1111/j.1750-3841.2012.02811.x

    Article  CAS  PubMed  Google Scholar 

  38. Gänzle MG, Vermeulen N, Vogel RF (2007) Carbohydrate, peptide and lipid metabolism of lactic acid bacteria in sourdough. Food Microbiol 24:128–138. https://doi.org/10.1016/j.fm.2006.07.006

    Article  CAS  PubMed  Google Scholar 

  39. Collins YF, McSweeney PLH, Wilkinson MG (2003) Lipolysis and free fatty acid catabolism in cheese: a review of current knowledge. Int Dairy J 13:841–866. https://doi.org/10.1016/S0958-6946(03)00109-2

    Article  CAS  Google Scholar 

  40. Thierry A, Collins YF, Abeijón Mukdsi MC, et al (2017) Lipolysis and metabolism of fatty acids in cheese. In: McSweeney PLH, Fox PF, Cotter PD, Everett DW (eds) Cheese. Elsevier, Amsterdam, pp 423–444

    Chapter  Google Scholar 

  41. Caplice E, Fitzgerald GF (1999) Food fermentations: role of microorganisms in food production and preservation. Int J Food Microbiol 50:131–149. https://doi.org/10.1016/S0168-1605(99)00082-3

    Article  CAS  PubMed  Google Scholar 

  42. Stiles ME (1996) Biopreservation by lactic acid bacteria. Antonie Van Leeuwenhoek 70:331–345. https://doi.org/10.1007/BF00395940

    Article  CAS  PubMed  Google Scholar 

  43. Moretti A, Susca A (2017) Mycotoxigenic fungi. Springer, New York

    Book  Google Scholar 

  44. Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, Boston

    Book  Google Scholar 

  45. Leyva Salas M, Mounier J, Valence F et al (2017) Antifungal microbial agents for food biopreservation—a review. Microorganisms 5:37. https://doi.org/10.3390/microorganisms5030037

    Article  CAS  PubMed Central  Google Scholar 

  46. Bianchini A (2015) Lactic acid bacteria as antifungal agents. In: Holzapfel W (ed) Advances in fermented foods and beverages. Woodhead Publishing, Cambridge, pp 333–353

    Chapter  Google Scholar 

  47. Crowley S, Mahony J, van Sinderen D (2013) Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci Technol 33:93–109. https://doi.org/10.1016/j.tifs.2013.07.004

    Article  CAS  Google Scholar 

  48. Lavermicocca P, Valerio F, Evidente A et al (2000) Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl Environ Microbiol 66:4084–4090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Schnürer J, Magnusson J (2005) Antifungal lactic acid bacteria as biopreservatives. Trends Food Sci Technol 16:70–78. https://doi.org/10.1016/j.tifs.2004.02.014

    Article  CAS  Google Scholar 

  50. Varsha KK, Nampoothiri KM (2016) Appraisal of lactic acid bacteria as protective cultures. Food Control 69:61–64. https://doi.org/10.1016/j.foodcont.2016.04.032

    Article  CAS  Google Scholar 

  51. EFSA (2011) Scientific opinion on risk based control of biogenic amine formation in fermented foods: biogenic amines in fermented foods. EFSA J 9:2393. https://doi.org/10.2903/j.efsa.2011.2393

    Article  CAS  Google Scholar 

  52. Santos MHS (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231. https://doi.org/10.1016/0168-1605(95)00032-1

    Article  CAS  Google Scholar 

  53. Spano G, Russo P, Lonvaud-Funel A et al (2010) Biogenic amines in fermented foods. Eur J Clin Nutr 64:S95–S100. https://doi.org/10.1038/ejcn.2010.218

    Article  CAS  PubMed  Google Scholar 

  54. Elsanhoty RM, Ramadan MF (2016) Genetic screening of biogenic amines production capacity from some lactic acid bacteria strains. Food Control 68:220–228. https://doi.org/10.1016/j.foodcont.2016.04.002

    Article  CAS  Google Scholar 

  55. Brandt MJ (2014) Starter cultures for cereal based foods. Food Microbiol 37:41–43. https://doi.org/10.1016/j.fm.2013.06.007

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by scientific internship provided by the Algerian Ministry of Higher Education and Scientific Research in CIRM-BIA, UMR1253 INRA-Rennes, France.

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Authors and Affiliations

  1. Department of Cellular and Molecular Biology, University of Abbes Laghrour, 40000, Khenchela, Algeria

    Ryma Merabti

  2. Laboratory of Biotechnology and Food Quality, Institute of Nutrition, Food and Agri-Food Technologies (INATAA), University of Constantine 1, 25000, Constantine, Algeria

    Ryma Merabti, Fatima Zohra Becila, Rania Boussekine & Farida Bekhouche

  3. STLO, Agrocampus Ouest, INRA, 35000, Rennes, France

    Marie N. Madec, Victoria Chuat & Florence Valence

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  1. Ryma Merabti
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Merabti, R., Madec, M.N., Chuat, V. et al. First Insight into the Technological Features of Lactic Acid Bacteria Isolated from Algerian Fermented Wheat Lemzeiet. Curr Microbiol 76, 1095–1104 (2019). https://doi.org/10.1007/s00284-019-01727-3

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