1887

Microbiology Society logo

Volume 167, Issue 1

Lactic acid bacterial exopolysaccharides strongly bind histamine and can potentially be used to remove histamine contamination in food Free

Abstract

The symptoms of foodborne histamine poisoning are similar to those of IgE-mediated food allergies. In this study, we investigated the histamine-binding capacity of lactic acid bacteria (LAB) strains as potential preventive agents against histamine poisoning. Histamine biosorption capacity was determined for 16 LAB strains. TOKAI 51 m, TOKAI 65 m, TOKAI 111 m and TOKAI 759 m showed especially high biosorption rates and reached saturation within 30 min. Adsorption isotherms showed better conformance to the Freundlich model than to the Langmuir model. Analyses after heat, periodic acid and guanidine hydrochloride treatments suggested that histamine was bound to the bacterial cell surface. HPLC analysis revealed that exopolysaccharides produced by TOKAI 65 m strongly bound to histamine. In the detachment test with 1 mol l HCl solution, the dissociation rate of histamine for TOKAI 65 m was <10 %. This strain is presumably a suitable candidate for use against histamine poisoning.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biogenic amine , biosorption , detoxification , exopolysaccharide , histamine and lactic acid bacteria
© 2021 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000936
2020-12-02
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/167/1/micro000936.html?itemId=/content/journal/micro/10.1099/mic.0.000936&mimeType=html&fmt=ahah

References

  1. Bjornsdottir-Butler K, McCarthy SA, Dunlap PV, Benner RA. Photobacterium angustum and Photobacterium kishitanii, psychrotrophic high-level histamine-producing bacteria indigenous to tuna. Appl Environ Microbiol 2016; 82:2167–2176 [View Article][PubMed]
     [Google Scholar]
  2. Dalgaard P, Madsen HL, Samieian N, Emborg J. Biogenic amine formation and microbial spoilage in chilled garfish (Belone belone belone)-effect of modified atmosphere packaging and previous frozen storage. J Appl Microbiol 2006; 101:80–95 [View Article][PubMed]
     [Google Scholar]
  3. Visciano P, Schirone M, Tofalo R, Suzzi G. Histamine poisoning and control measures in fish and fishery products. Front Microbiol 2014; 5:500 [View Article][PubMed]
     [Google Scholar]
  4. Prester L. Biogenic amines in fish, fish products and shellfish: a review. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2011; 28:1547–1560 [View Article][PubMed]
     [Google Scholar]
  5. Feord J. Lactic acid bacteria in a changing legislative environment. Antonie van Leeuwenhoek 2002; 82:353–360 [View Article][PubMed]
     [Google Scholar]
  6. Nowak A, Kuberski S, Libudzisz Z. Probiotic lactic acid bacteria detoxify N-nitrosodimethylamine. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2014; 31:1678–1687 [View Article][PubMed]
     [Google Scholar]
  7. Huang W, Chang J, Wang P, Liu C, Yin Q et al. Effect of the combined compound probiotics with mycotoxin-degradation enzyme on detoxifying aflatoxin B1 and zearalenone. J Toxicol Sci 2018; 43:377–385 [View Article][PubMed]
     [Google Scholar]
  8. Turbic A, Ahokas JT, Haskard CA. Selective in vitro binding of dietary mutagens, individually or in combination, by lactic acid bacteria. Food Addit Contam 2002; 19:144–152 [View Article][PubMed]
     [Google Scholar]
  9. Bajpai VK, Rather IA, Majumder RM, Shukla S, Aeron A et al. Exopolysaccharide and lactic acid bacteria: perception, functionality and prospects. Bangladesh J Pharmacol 2017; 11:1–23 [View Article]
     [Google Scholar]
  10. Nybom SM, Dziga D, Heikkilä JE, Kull TP, Salminen SJ et al. Characterization of microcystin-LR removal process in the presence of probiotic bacteria. Toxicon 2012; 59:171–181 [View Article][PubMed]
     [Google Scholar]
  11. Heikkilä JE, Nybom SM, Salminen SJ, Meriluoto JA. Removal of cholera toxin from aqueous solution by probiotic bacteria. Pharmaceuticals 2012; 5:665–673 [View Article][PubMed]
     [Google Scholar]
  12. Kinoshita H, Sohma Y, Ohtake F, Ishida M, Kawai Y et al. Biosorption of heavy metals by lactic acid bacteria and identification of mercury binding protein. Res Microbiol 2013; 164:701–709 [View Article][PubMed]
     [Google Scholar]
  13. Kinoshita H, Ohtake F, Ariga Y, Kimura K. Comparison and characterization of biosorption by Weissella viridescens MYU 205 of periodic group 12 metal ions. Anim Sci J 2016; 87:271–276 [View Article][PubMed]
     [Google Scholar]
  14. Kinoshita H, Sato Y, Ohtake F, Ishida M, Komoda T et al. In vitro mass-screening of lactic acid bacteria as potential biosorbents of cesium and strontium ions. J Microbiol Biotech Food Sci 2015; 04:383–386 [View Article]
     [Google Scholar]
  15. Pessione E, Cirrincione S. Bioactive molecules released in food by lactic acid bacteria: encrypted peptides and biogenic amines. Front Microbiol 2016; 7:876 [View Article][PubMed]
     [Google Scholar]
  16. Landete JM, Ferrer S, Pardo I. Which lactic acid bacteria are responsible for histamine production in wine?. J Appl Microbiol 2005; 99:580–586 [View Article][PubMed]
     [Google Scholar]
  17. Coton M, Romano A, Spano G, Ziegler K, Vetrana C et al. Occurrence of biogenic amine-forming lactic acid bacteria in wine and cider. Food Microbiol 2010; 27:1078–1085 [View Article][PubMed]
     [Google Scholar]
  18. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H et al. Biogenic amines in fermented foods. Eur J Clin Nutr 2010; 64:S95–S100 [View Article][PubMed]
     [Google Scholar]
  19. Mazzoli R, Lamberti C, Coisson JD, Purrotti M, Arlorio M et al. Influence of ethanol, malate and arginine on histamine production of Lactobacillus hilgardii isolated from an Italian red wine. Amino Acids 2009; 36:81–89 [View Article][PubMed]
     [Google Scholar]
  20. Fernández M, del Río B, Linares DM, Martín MC, Alvarez MA. Real-Time polymerase chain reaction for quantitative detection of histamine-producing bacteria: use in cheese production. J Dairy Sci 2006; 89:3763–3769 [View Article][PubMed]
     [Google Scholar]
  21. Callejón S, Sendra R, Ferrer S, Pardo I. Identification of a novel enzymatic activity from lactic acid bacteria able to degrade biogenic amines in wine. Appl Microbiol Biotechnol 2014; 98:185–198 [View Article][PubMed]
     [Google Scholar]
  22. Callejón S, Sendra R, Ferrer S, Pardo I. Cloning and characterization of a new laccase from Lactobacillus plantarum J16 CECT 8944 catalyzing biogenic amines degradation. Appl Microbiol Biotechnol 2016; 100:3113–3124 [View Article][PubMed]
     [Google Scholar]
  23. García-Ruiz A, González-Rompinelli EM, Bartolomé B, Moreno-Arribas MV. Potential of wine-associated lactic acid bacteria to degrade biogenic amines. Int J Food Microbiol 2011; 148:115–120 [View Article][PubMed]
     [Google Scholar]
  24. Capozzi V, Russo P, Ladero V, Fernández M, Fiocco D et al. Biogenic amines degradation by Lactobacillus plantarum: toward a potential application in wine. Front Microbiol 2012; 3:122 [View Article][PubMed]
     [Google Scholar]
  25. Volesky B. Biosorption of heavy metals. CRC Press 19907–44
     [Google Scholar]
  26. Hassan SH, Kim SJ, Jung AY, Joo JH, Eun Oh S et al. Biosorptive capacity of Cd(II) and Cu(II) by lyophilized cells of Pseudomonas stutzeri . J Gen Appl Microbiol 2009; 55:27–34 [View Article][PubMed]
     [Google Scholar]
  27. Tian F, Zhai Q, Zhao J, Liu X, Wang G et al. Lactobacillus plantarum CCFM8661 alleviates lead toxicity in mice. Biol Trace Elem Res 2012; 150:264–271 [View Article][PubMed]
     [Google Scholar]
  28. Zhai Q, Wang G, Zhao J, Liu X, Tian F et al. Protective effects of Lactobacillus plantarum CCFM8610 against acute cadmium toxicity in mice. Appl Environ Microbiol 2013; 79:1508–1515 [View Article][PubMed]
     [Google Scholar]
  29. Liu Z, Zhang Z, Qiu L, Zhang F, Xu X et al. Characterization and bioactivities of the exopolysaccharide from a probiotic strain of Lactobacillus plantarum WLPL04. J Dairy Sci 2017; 100:6895–6905 [View Article][PubMed]
     [Google Scholar]
  30. Ziadi M, Bouzaiene T, M'Hir S, Zaafouri K, Mokhtar F et al. Evaluation of the efficiency of ethanol precipitation and ultrafiltration on the purification and characteristics of exopolysaccharides produced by three lactic acid bacteria. Biomed Res Int 2018; 2018:1896240 [View Article][PubMed]
     [Google Scholar]
  31. Wang B, Song Q, Zhao F, Zhang L, Han Y et al. Isolation and characterization of dextran produced by Lactobacillus sakei L3 from Hubei sausage. Carbohydr Polym 2019; 223:115111 [View Article][PubMed]
     [Google Scholar]
  32. Gupta P, Diwan B. Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 2017; 13:58–71 [View Article][PubMed]
     [Google Scholar]
  33. Polak-Berecka M, Szwajgier D, Waśko A, Al Bof. Biosorption of Al(+3) and Cd(+2) by an exopolysaccharide from Lactobacillus rhamnosus . J Food Sci 2014; 79:T2404–2408 [View Article][PubMed]
     [Google Scholar]
  34. Pigeon RM, Cuesta EP, Gililliand SE. Binding of free bile acids by cells of yogurt starter culture bacteria. J Dairy Sci 2002; 85:2705–2710 [View Article][PubMed]
     [Google Scholar]
  35. Makino S, Ikegami S, Kano H, Sashihara T, Sugano H et al. Immunomodulatory effects of polysaccharides produced by Lactobacillus delbrueckii sp. bulgaricus OLL1073R-1. J Dairy Sci 2006; 89:2873–2881 [View Article][PubMed]
     [Google Scholar]
  36. Shi QH, Shen FF, Sun S. Studies of lysozyme binding to histamine as a ligand for hydrophobic charge induction chromatography. Biotechnol Prog 2010; 26:134–141 [View Article][PubMed]
     [Google Scholar]
  37. Guarcello R, De Angelis M, Settanni L, Formiglio S, Gaglio R et al. Selection of amine-oxidizing dairy lactic acid bacteria and identification of the enzyme and gene involved in the decrease of biogenic amines. Appl Environ Microbiol 2016; 82:6870–6880 [View Article][PubMed]
     [Google Scholar]
  38. Fadda S, Vignolo G, Oliver G. Tyramine degradation and tyramine/histamine production by lactic acid bacteria and Kocuria strains. Biotechnol Let 2001; 23:2015–2019 [View Article]
     [Google Scholar]
  39. Xu Y, Liu Y, Xu B, Wang D, Jiang W. Characterisation and application of Halomonas shantousis SWA25, a halotolerant bacterium with multiple biogenic amine degradation activity. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2016; 33:674–682 [View Article][PubMed]
     [Google Scholar]
  40. Bäumlisberger M, Moellecken U, König H, Claus H. The potential of the yeast Debaryomyces hansenii H525 to degrade biogenic amines in food. Microorganisms 2015; 3:839–850 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000936
Loading
Lactic acid bacterial exopolysaccharides strongly bind histamine and can potentially be used to remove histamine contamination in food
Microbiology 167, 000936 (2021); https://doi.org/10.1099/mic.0.000936
/content/journal/micro/10.1099/mic.0.000936
/content/journal/micro/10.1099/mic.0.000936
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error