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Functional Properties of Lactic Acid Bacteria Isolated from Ethnic Fermented Vegetables of the Himalayas

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Functional Properties of Lactic Acid Bacteria Isolated from Ethnic Fermented Vegetables of the Himalayas International Journal of Food Microbiology 135 (2009) 28–33 Contents lists available at ScienceDirect International Journal of Food Microbiology journal homepage: www.elsevier.com/locate/ijfoodmicro Functional properties of lactic acid bacteria isolated from ethnic fermented vegetables of the Himalayas Jyoti Prakash Tamang a,⁎, Buddhiman Tamang a, Ulrich Schillinger b, Claudia Guigas b, Wilhelm H. Holzapfel b a Food Microbiology Laboratory, Department of Microbiology, Sikkim University, 6th Mile, Tadong 737102, Sikkim, India b Institute of Hygiene and Toxicology, Federal Research Centre for Nutrition and Foods, Haid-und-Neu-Str. 9, D-76131 Karlsruhe, Germany article info abstract Article history: A total of 94 strains of Lactic acid bacteria (LAB), previously isolated from ethnic fermented vegetables and Received 26 March 2009 tender bamboo shoots of the Himalayas, were screened for functional properties such as acidification Received in revised form 15 July 2009 capacity, enzymatic activities, degradation of antinutritive factors and oligosaccharides, production of Accepted 15 July 2009 biogenic amines, hydrophobicity and adherence to mucus secreting HT29 MTX cells. Strong acidification and coagulation activities of LAB strains were recorded. Most of the LAB strains showed antimicrobial activities Keywords: against the used indicator strains; however, only Lb. plantarum IB2 (BFE 948) isolated from inziangsang, a Functional properties LAB fermented leafy vegetable product, produced a bacteriocin against Staphylococcus aureus S1. LAB strains Fermented vegetables showed enzymatic activities and also degraded oligosaccharides. Almost all the strains of LAB were non- Himalayas producers of biogenic amines except few strains. Some strains of Lb. plantarum showed more than 70% hydrophobicity. Adherence to the mucus secreting HT29 MTX cells was also shown by seven strains indicating their probiotic nature. © 2009 Elsevier B.V. All rights reserved. 1. Introduction alcoholic beverages (Thapa and Tamang, 2004). The functional proper- ties of LAB are important for selection of appropriate strains to be used as Lactic acid bacteria (LAB) are the dominant microorganisms in starter culture (Durlu-Ozkaya et al., 2001; Badis et al., 2004). ethnic fermented vegetables and bamboo shoot products of the Industrialised countries have benefited from a century of experience Himalayas (Tamang, 2009). Gundruk, sinki and khalpi are lactic with starter cultures, particularly selected for large scale food fermented vegetable products of Nepal, Darjeeling hills, Sikkim and fermentation (Holzapfel et al., 1998). The present paper aims to study Bhutan (Tamang et al., 1988), and inziangsang is a fermented leafy the functional properties of LAB from ethnic fermented vegetables vegetable product of Nagaland and Manipur (Tamang and Tamang, and tender bamboo shoots which include acidifying and coagulating 2009). The LAB involved in these ethnic fermented vegetables were capacity, antimicrobial activities, degradation of phytic acid, utilization identified as Lactobacillus brevis, Lactobacillus plantarum, Pediococcus of oligosaccharides, and adherence to hydrocarbons and intestinal pentosaceus, Pediococcus acidilactici and Leuconostoc fallax (Tamang mucosa. et al., 2005). Predominant functional LAB strains associated with the ethnic fermented tender bamboo shoot products, mesu, soidon, soibum and soijim of the Himalayas, were identified as Lb. brevis, Lb. plantarum, 2. Materials and methods Lb. curvatus, P. pentosaceus, Leuc. mesenteroides subsp. mesenteroides, Leuc. fallax, Leuc. lactis, Leuc. citreum and Enterococcus durans (Tamang 2.1. LAB strains studied et al., 2008). Some of the LAB strains may also possess protective and functional properties, which render them interesting candidates for use A total of 94 strains of LAB were studied for various functional as starter culture(s) for controlled and optimised production of properties. Out of which, 38 strains were previously isolated from ethnic fermented vegetable products. Though ethnic fermented foods are fermented vegetables of the Himalayas: gundruk (12 strains), sinki (10), widely prepared and consumed in the Himalayas, application of khalpi (12) and inziangsang (4); and 56 strains were isolated from the standard starter culture is not a tradition except for production of Himalayan fermented bamboo shoot products: mesu (35 strains), soibum (7), soidon (7), and soijim (7). These LAB strains were phenotypically and genotypically identified as Lb. brevis, Lb. plantarum, Lb. curvatus, P. pentosaceus, P. acidilactici, Leuc. mesenteroides subsp. ⁎ Corresponding author. Department of Microbiology, Sikkim University, 6th Mile, Tadong 737102, Sikkim, India. Tel.: +91 3592 231053, +91 9832061073 (Mobile). mesenteroides, Leuc. fallax, Leuc. lactis, Leuc. citreum and E. durans E-mail address: [email protected] (J.P. Tamang). (Tamang et al., 2005, 2008). 0168-1605/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.ijfoodmicro.2009.07.016 J.P. Tamang et al. / International Journal of Food Microbiology 135 (2009) 28–33 29 2.2. Acidification and coagulation containing 2% stachyose and 1% raffinose (instead of glucose), respectively, and 0.004% chlorophenol red as indicator. Inocula- Acidification and coagulation properties were assayed by inocu- tion was followed by incubation at 30 °C for 3 days (Holzapfel, lating 10% skim milk (RM1254, HiMedia, India) with LAB strains. 1997). Observation was made for commencement of clotting, and the pH was measured after 72 h of incubation at 30 °C (Olasupo et al., 2001). 2.7. Biogenic amines 2.3. Antimicrobial activity The ability of LAB strains to produce biogenic amines was deter- The LAB strains were screened for antimicrobial activity by the mined qualitatively in screening medium (Bover-Cid and Holzapfel, agar spot method of Schillinger and Lücke (1989). The indicator 1999) using a ‘cocktail’ of four precursor amino acids (histidine, ly- strains used for antagonisms included: Listeria innocua DSM 20649, sine, ornithine and tyrosine). Change of the bromocresol purple indi- L. monocytogenes DSM 20600, Bacillus cereus CCM 2010, Staphylococ- cator to purple was considered as index of significant amino acid cus aureus S1, Enterococcus faecium DSM 20477, Streptococcus mutans decarboxylase activity, corresponding to N350 mg of a particular DSM 6178, Klebsiella pneumoniae subsp. pneumoniae BFE 147, Enter- amino acid/litre (Olasupo et al., 2001). obacter cloacae BFE 282, E. agglomerans BFE 154 and Pseudomonas aeruginosa BFE 162. Cell-free neutralised supernatant fluids of LAB strains were screened for antimicrobial activity by the agar spot test 2.8. Hydrophobicity assay (Uhlman et al., 1992), using the bacteriocin screening medium (MRS agar containing only 0.2% glucose) as described by Tichaczek et al. Bacterial adhesion to hydrocarbons was determined and results (1992). were expressed according to Rosenberg (1984), modified as follows. Bacteriocin activity was quantified based on an agar diffusion Fresh cultures were grown in MRS broth at 30 °C for 24 h and centri- assay as described by Cabo et al. (1999). The twofold serial dilutions of fuged at 8000 ×g for 5 min. The pellet was washed three times with the neutralised supernatants are spotted (10 μl) onto the surface of 9 ml of quarter strength Ringer's Solution (QSRS) (Merck, Germany), MRS or Standard I Nutrient agar containing the required indicator and thoroughly mixed in a vortex. 1 ml of the suspension was taken bacteria. Bacteriocin titres were expressed as the reciprocal of the and the absorbance at 580 nm was measured. Then, 1.5 ml of the highest dilution exhibiting a zone of inhibition and were reported in suspension was mixed with equal volume of n-hexadecane (RM 2238, activity units (AU) per ml. HiMedia, India) in duplicates and mixed thoroughly in a vortex. The phases were allowed to separate for 1 h at room temperature, after 2.4. Enzymatic activities which the aqueous phase was carefully removed and absorbance at 580 nm was measured. The percentage hydrophobicity was expressed The enzymatic activities of LAB strains were assayed using the as follows: hydrophobicity %=[A0 −A/A]×100, where A0 and A are commercial API-zym (bioMérieux, France) galleries. Cultures were the absorbance values of the aqueous phase before and after contact grown on MRS agar and cells were harvested in 2 ml sterile normal with n-hexadecane hydrophobicity determinations were done in saline which was used to prepare a suspension of 107 cells/ml. The three replicates. The percent hydrophobic index greater than 70% was strip was unpacked and 2 drops of cell suspensions were inoculated arbitrarily classified as hydrophobic (Martin et al., 1989; Nostro et al., in each cupule of the strip containing ready-made enzyme substrates 2004). and incubated at 30 °C for 6 h. After incubation, 1 drop of ready-made zym-A and zym-B reagents was added and observed for colour development based on the manufacturer's colour chart. A value 2.9. In vitro adherence assay ranging from 0–5 were assigned, corresponding to the colours developed: 0 corresponds to a negative reaction, 5 ( =40 nanomoles) Mucus secreting HT29 MTX cells (clone 5M21) obtained from to a reaction of maximum intensity, and values 4, 3, 2 and 1 were Dr. Thecla Lessuffleur (INSERM U178, Villejuif, France) were used. intermediate reactions corresponding to 30, 20, 10 and 5 nanomoles, Cells were routinely grown in Dulbecco's modified Eagles minimal respectively. essential medium
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