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Molecular characterization of non-biogenic amines producing Lactobacillus plantarum GP11 isolated from traditional pickles using HRESI-MS analysis

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Abstract

Fungal spoilage and toxic biogenic amine production is a major risk in fermented products. Therefore, the selection of nontoxic biogenic amines producing probiotic bacteria plays a vital role in the fermentation process. In the present study, a total of 18 bacterial isolates were isolated from eight different homemade pickle samples and 15 lactic acid bacteria (LAB) were identified based on biochemical tests. Out of which only seven isolates (GP1, GP2, GP3, GP4, GP5, GP9, and GP11) exhibited antifungal activity against pickle contaminant Aspergillus sp and Penicillium sp. Among the potential LAB isolates, GP11 showed the highest antifungal activity against Aspergillus sp and Penicillium sp with a zone of inhibition 28.33 ± 0.57and 19.66 ± 0.57 mm respectively. The potent LAB isolates were tested for amino acid decarboxylase activity, in which GP2, GP3, GP4, and GP5 exhibited to produce tyramine, cadaverine, and phenylethylamine while GP1 and GP5 have produced tyramine and phenylethylamine respectively. However, highly potent antifungal active isolate GP11 did not produce biogenic amine. Further, GP1, GP9, and GP11 were subjected to confirmation of biogenic amines production using HRESI-MS. HRESI-MS analysis of the GP1 and GP9 sample confirmed the presence of phenylethylamine and tyramine respectively. Interestingly, GP11 isolate did not show any biogenic amines production and GP11 was further subjected to 16S rRNA typing and identified as Lactobacillus plantarum. On in situ pickle sensory evaluation, GP11 lactopickle was graded as very good quality when compared to traditional one. Therefore L. plantarum GP11 could be developed as an ideal starter culture for the fermented production of a pickle.

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References

  • Alberto MR, Arena ME, de Nadra MCM (2002) A comparative survey of two analytical methods for identification and quantification of biogenic amines. Food Control 13:125–129

    Article  CAS  Google Scholar 

  • Aysun CSM, Demirkol O, Ayhan K (2017) Amino acid decarboxylase activities and biogenic amine formation abilities of lactic acid bacteria isolated from shalgam. Int J Food Prop 20:171–178. https://doi.org/10.1080/10942912.2016.1152479

    Article  CAS  Google Scholar 

  • Barkai-Golan R (2008) Penicillium mycotoxins. Mycotoxins Fruits Vegetables. https://doi.org/10.1016/b978-0-12-374126-4.00007-3

    Article  Google Scholar 

  • Bonczar G, Filipczak-Fiutak M, Pluta-Kubica A, Duda I, Walczycka M, Staruch L (2018) The range of protein hydrolysis and biogenic amines content in selected acid- and rennet-curd cheeses. Chem Pap 72:2599–2606

    Article  CAS  Google Scholar 

  • Bryla M, Wáskiewicz A, Podolska G, Szymczyk K, Jedrzejczak R, Damaziak K, Sułek A (2016) Occurrence of 26 mycotoxins in the grain of cereals cultivated in Poland. Toxins 8:160. https://doi.org/10.3390/toxins8060160

    Article  CAS  PubMed Central  Google Scholar 

  • Cabo ML, Braber AF, Koenraad PMFJ (2002) Apparent antifungal activity of several lactic acid bacteria against Penicilliumdiscolor is due to acetic acid in the medium. J Food Protec 65:1309–1316

    Article  CAS  Google Scholar 

  • Capozzi V, Russo P, Ladero V, Fernández M, Fiocco D, Alvarez MA, Grieco F, Spano G (2012) Biogenic amines degradation by lactobacillus plantarum: toward a potential application in wine. Front Microbiol 3:122. https://doi.org/10.3389/fmicb.2012.00122

    Article  PubMed  PubMed Central  Google Scholar 

  • Cunha SC, Faria MA, Fernandes JO (2011) Gas chromatography-mass spectrometry assessment of amines in Port wine and grape juice after fast chloroformate extraction/derivatization. J Agric Food Chem 59:8742–8753

    Article  CAS  Google Scholar 

  • Dallal MS, Zamaniahari S, Davoodabadi A, Hosseini M, Rajabi Z (2017) Identification and characterization of probiotic lactic acid bacteria isolated from traditional Persian pickled vegetables. GMS Hyg Infect Control 12:1–8

    Google Scholar 

  • Dangmance N, Chumkeaw N, Munkhun R, Boonson J (2015) Isolation of lactic acid bacteria from pickled cabbage for probiotic characterization. BHST 13:63–66

    Google Scholar 

  • Dapkevicius MLE, Nout MR, Rombouts FM, Houben JH, Wymenga W (2000) Biogenic amine formation and degradation by potential fish silage starter microorganisms. Inter J Food Microbial 57:107–114

    Article  CAS  Google Scholar 

  • De Llano DG (1998) Biogenic amine production by wild lactococcal and leuconostoc strains. Lett Appl Microbial 26:270–274

    Article  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–469. https://doi.org/10.1093/nar/gkn180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doeun D, Davaatseren M, Chung M-S (2017) Biogenic amines in foods. Food Sci Biotechnol 26:1463–1474

    Article  CAS  Google Scholar 

  • Fang F, Feng T, Du G, Chen (2016) Evaluation of the impact on food safety of a Lactobacillus coryniformis strain from pickled vegetables with degradation activity against nitrite and other undesirable compounds. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 33:623–630

    CAS  PubMed  Google Scholar 

  • Garai G, Dueñas MT, Irastorza A, Moreno-Arribas MV (2007) Biogenic amine production by lactic acid bacteria isolated from cider. Lett Appl Microbiol 45:473–478

    Article  CAS  Google Scholar 

  • Gashe BA, Mpuchane S, Matsheka MI, Magwamba CC (2013) Biogenic amine producing bacteria associated with three different commercially fermented beverages in Botswana. Afri J Microbiol Res 7:342–350

    Article  Google Scholar 

  • Huh CK, Hwang TY (2016) Identification of antifungal substances of Lactobacillus sakei subsp. ALI033 and antifungal activity against Penicillium brevicompactum strain FI02. Prev Nutr Food Sci 21:52

    Article  CAS  Google Scholar 

  • Hussain H, MohdFuat AR, Vimala B, Ghazali HM (2011) Screening method for detection of immediate amino acid decarboxylases-producing bacteria implicated in food poisoning. Trop Biomed 28:351–361

    PubMed  Google Scholar 

  • Innocente N, Dágostin P (2002) Formation of biogenic amines in a typical semihard Italian cheese. J Food Protect 65:1498–1501

    Article  CAS  Google Scholar 

  • Kalagatur NK, Kamasani JR, Mudili V (2018) Assessment of detoxification efficacy of irradiation on zearalenone mycotoxin in various fruit juices by response surface methodology and elucidation of its in vitro toxicity. Front Microbiol 9:2937. https://doi.org/10.3389/fmicb.2018.02937

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim J-D (2005) Antifungal activity of Lactic Acid Bacteria isolated from Kimchi against Aspergillus fumigatus. Mycobiology 33(4):210–214

    Article  CAS  Google Scholar 

  • Kongkiattikajorn J (2015) Effect of ginger extract to inhibit biogenic amines accumulation during nham fermentation. J Food Chem Nanotechnol 1:15–19

    Article  Google Scholar 

  • Marcia LS, Thierry A, Lemaître M, Garric G, Harel-Oger M, Chatel M, Lê S, Mounier J, Valence F, Coton E (2018) Antifungal activity of lactic acid bacteria combinations in dairy mimicking models and their potential as bioprotective cultures in pilot scale applications. Front Microbiol 9:1787. https://doi.org/10.3389/fmicb.2018.01787

    Article  Google Scholar 

  • MerihKivanc KS, Pektas S (2014) Screening of lactic acid bacteria for antifungal activity against fungi. J Food Process Technol 5:310. https://doi.org/10.4172/2157-7110.1000310

    Article  Google Scholar 

  • Moracanin SV, Stefanovic S, Radicevic T, Borovic B, Djukic D (2015) Production of biogenic amines by lactic acid bacteria isolated from Uzicka sausages. Procedia Food Sci 5:308–311

    Article  Google Scholar 

  • Moret S, Smela D, Populin T, Conte LS (2005) A survey of biogenic amine content of fresh and preserved vegetables. Food Chem 89:355–361

    Article  CAS  Google Scholar 

  • Nalazek-Rudnicka K, Wasik A (2017) Development and validation of an LC–MS/MS method for the determination of biogenic amines in wines and beers. Monatsh Chem 148:1685–1696

    Article  CAS  Google Scholar 

  • Önal A (2007) A review: current analytical methods for the determination of biogenic amines in foods. Food Chem 103:1475–1486

    Article  Google Scholar 

  • Ono H, Shoko N, Tsurii J, Kawamoto T, Sonomoto K, Nakayama J (2014) Monitoring of the microbiota profile in nukadoko, a naturally fermented rice bran bed for pickling vegetables. J Biosci Bioeng 20:1–6

    Google Scholar 

  • Priyadarshani WD, Rakshit SK (2014) Growth and biogenic amine (histamine and tyramine) potential of probiotic Lactobacillus casei in skim milk. Am J Food Technol 9:69–79

    Article  CAS  Google Scholar 

  • Rodriguez MBR, Da Silva CC, Da Silva Feijó MB, Júnior CAC, Mano SB (2014) Bioactive amines: aspects of quality and safety in food. Food Nutri Sci 5:138

    Google Scholar 

  • Sagratini G, Fernández-Franzón M, De Berardinis F, Font G, Vittori S, Mañes J (2012) Simultaneous determination of eight underivatized biogenic amines in fish by solid-phase extraction and liquid chromatography-tandem mass spectrometry. Food Chem 132:537–543

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sentellas S, Nunez O, Saurina J (2016) Recent advances in the determination of biogenic amines in food samples by (U) HPLC. J Agric Food Chem 64:7667–7678

    Article  CAS  Google Scholar 

  • Shiling L, Caihong J, Xinglian X, Chengjian X, Kaixiong L, Ruihua S (2015) Improved screening procedure for Biogenic amine production by Lactic Acid Bacteria and Enterobacteria. Czech J Food Sci 33:1–8

    Google Scholar 

  • Singh VP, Pathak V, Verma AK (2012) Fermented meat products: organoleptic qualities and biogenic amines–a review. Am J Food Technol 7:278–288. https://doi.org/10.3923/ajft.2012.278.288

    Article  CAS  Google Scholar 

  • Swamy CT, Gayathri D, Devaraja TN, Bandekar M, D’Souza SE, Meena RM, Ramaiah N (2016) Plant growth promoting potential and phylogenetic characteristics of a lichenized nitrogen fixing bacterium Enterobacter cloacae. JBM 56:1369–1379

    CAS  Google Scholar 

  • Xue H, Huaxi Y, Lanwei Z, Weiwei H, Yingchun Z, Lili Z, Ming D (2014) Improvement of fermented chinese cabbage characteristics by selected starter cultures. J Food Sci. https://doi.org/10.1111/1750-3841.12495

    Article  PubMed  Google Scholar 

  • Yu J, Gao W, Qing M, Sun Z, Wang W, Liu W, Pan P, Sun T, Wang H, Bai N, Zhang H (2012) Identification and characterization of lactic acid bacteria isolated from traditional pickles in Sichuan, China. J Gen Appl Microbio 58:163–172

    Article  CAS  Google Scholar 

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P V Research student, executed the planned experimental work. A R Helped in analysing data. D G Research supervisor, developed the idea, planned the experimental design and prepared the manuscript. M V Helped in the experimentation process and manuscript preparation.

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Correspondence to Devaraja Gayathri.

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Priyanka, V., Ramesha, A., Gayathri, D. et al. Molecular characterization of non-biogenic amines producing Lactobacillus plantarum GP11 isolated from traditional pickles using HRESI-MS analysis. J Food Sci Technol 58, 2216–2226 (2021). https://doi.org/10.1007/s13197-020-04732-8

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