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Glucosinolate and Desulfo-glucosinolate Metabolism by a Selection of Human Gut Bacteria

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Abstract

Glucosinolate (GSL) hydrolysis is mediated by the enzyme myrosinase which together with specifier proteins can give rise to isothiocyanates (ITCs), thiocyanates, and nitriles (NITs) in cruciferous plants. However, little is known about the metabolism of GSLs by the human gut flora. The aim of the work was to investigate the metabolic fates of sinigrin (SNG), glucotropaeolin (GTP), gluconasturtiin (GNT), and their corresponding desulfo-GSLs (DS-GSLs). Three human gut bacterial strains, Enterococcus casseliflavus CP1, Lactobacillus agilis R16, and Escherichia coli VL8, were chosen for this study. GNT was metabolized to completion within 24 h to phenethyl ITC and phenethyl NIT (PNIT) by all bacteria, except for L. agilis R16 which produced only PNIT. At least 80 % of GTP and SNG were metabolized by all bacteria within 24 h to the corresponding ITCs and NITs. The pH of media over time gradually became acidic for both L. agilis R16 and E. coli VL8, while for E. casseliflavus CP1 the media became slightly alkaline with NIT and ITC production occurring between pH 3.0 and 7.5. ITC production peaked between 4 and 10 h in most cases and gradually declined while NIT production increased and remained relatively constant over time. The total percentage products accounted for 3–53 % of the initial GSL. NITs were produced from DS-GSLs suggesting an alternative metabolism via desulfation for the food based GSLs. The metal ion dependency for NIT production for GNT and its DS form was investigated where it was shown that Fe2+ increased NIT production, while Mg2+ stimulated the formation of ITC.

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References

  1. Agerbirk N, Olsen CE, Sorensen H (1998) Initial and final products, nitriles, and ascorbigens produced in myrosinase-catalyzed hydrolysis of indole glucosinolates. J Agric Food Chem 46:1563–1571

    Article  CAS  Google Scholar 

  2. Albaser A, Kazana E, Bennett MH, Cebeci F, Luang-In V, Spanu PD, Rossiter JT (2016) Discovery of a bacterial glycoside hydrolase family 3 (GH3) beta-glucosidase with myrosinase activity from a Citrobacter strain isolated from soil. J Agric Food Chem 64:1520–1527

    Article  CAS  PubMed  Google Scholar 

  3. Bellostas N, Petersen IL, Sorensen JC, Sorensen H (2008) A fast and gentle method for the isolation of myrosinase complexes from Brassicaceous seeds. J Biochem Biophys Methods 70:918–925

    Article  CAS  PubMed  Google Scholar 

  4. Bellostas N, Sorensen AD, Sorensen JC, Sorensen H (2008) Fe2+-catalyzed formation of nitriles and thionamides from intact glucosinolates. J Nat Prod 71:76–80

    Article  CAS  PubMed  Google Scholar 

  5. Bones AM, Rossiter JT (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 97:194–208

    Article  CAS  Google Scholar 

  6. Bones AM, Rossiter JT (2006) The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067

    Article  CAS  PubMed  Google Scholar 

  7. Burow M, Bergner A, Gershenzon J, Wittstock U (2007) Glucosinolate hydrolysis in Lepidium sativum—identification of the thiocyanate-forming protein. Plant Mol Biol 63:49–61

    Article  CAS  PubMed  Google Scholar 

  8. Cejpek K, Urban J, Velisek J, Hrabcova H (1998) Effect of sulphite treatment on allyl isothiocyanate in mustard paste. Food Chem 62:53–57

    Article  CAS  Google Scholar 

  9. Chen CW, Ho CT (1998) Thermal degradation of allyl isothiocyanate in aqueous solution. Agric Food Chem 46:220–223

    Article  CAS  Google Scholar 

  10. Cheng DL, Hashimoto K, Uda Y (2004) In vitro digestion of sinigrin and glucotropaeolin by single strains of Bifidobacterium and identification of the digestive products. Food Chem Toxicol 42:351–357

    Article  CAS  PubMed  Google Scholar 

  11. Combourieu B, Elfoul L, Delort AM, Rabot S (2001) Identification of new derivatives of sinigrin and glucotropaeolin produced by the human digestive microflora using H-1 NMR spectroscopy analysis of in vitro incubations. Drug Metab Dispos 29:1440–1445

    CAS  PubMed  Google Scholar 

  12. Cordeiro RP, Doria JH, Zhanel GG, Sparling R, Holley RA (2015) Role of glycoside hydrolase genes in sinigrin degradation by E. coli O157:H7. Int J Food Microbiol 205:105–111

    Article  CAS  PubMed  Google Scholar 

  13. de Souza CG, da Motta LL, de Assis AM, Rech A, Bruch R, Klamt F, Souza DO (2016) Sulforaphane ameliorates the insulin responsiveness and the lipid profile but does not alter the antioxidant response in diabetic rats. Food Funct 7:2060–2065

    Article  PubMed  Google Scholar 

  14. Elfoul L, Rabot S, Khelifa N, Quinsac A, Duguay A, Rimbault A (2001) Formation of allyl isothiocyanate from sinigrin in the digestive tract of rats monoassociated with a human colonic strain of Bacteroides thetaiotaomicron. FEMS Microbiol Lett 197:99–103

    Article  CAS  PubMed  Google Scholar 

  15. Folkard DL, Melchini A, Traka MH, Al-Bakheit A, Saha S, Mulholland F, Watson A, Mithen RF (2014) Suppression of LPS-induced transcription and cytokine secretion by the dietary isothiocyanate sulforaphane. Mol Nutr Food Res 58:2286–2296

    Article  CAS  PubMed  Google Scholar 

  16. Getahun SM, Chung FL (1999) Conversion of glucosinolates to isothiocyanates in humans after ingestion of cooked watercress. Cancer Epidemiol Biomark Prev 8:447–451

    CAS  Google Scholar 

  17. Hanschen FS, Brueggemann N, Brodehl A, Mewis I, Schreiner M, Rohn S, Kroh LW (2012) Characterization of products from the reaction of glucosinolate-derived isothiocyanates with cysteine and lysine derivatives formed in either model systems or broccoli sprouts. J Agric Food Chem 60:7735–7745

    Article  CAS  PubMed  Google Scholar 

  18. Hanschen FS, Lamy E, Schreiner M, Rohn S (2014) Reactivity and stability of glucosinolates and their breakdown products in foods. Angew Chem Int Ed 53:11430–11450

    Article  CAS  Google Scholar 

  19. Hasapis X, Macleod AJ (1982) Effects of metal-ions on benzylglucosinolate degradation in Lepidium sativum seed auto-lysates. Phytochemistry 21:559–563

    Article  CAS  Google Scholar 

  20. Jin Y, Wang MF, Rosen RT, Ho CT (1999) Thermal degradation of sulforaphane in aqueous solution. J Agric Food Chem 47:3121–3123

    Article  CAS  PubMed  Google Scholar 

  21. Jones AME, Bridges M, Bones AM, Cole R, Rossiter JT (2001) Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.). Insect Biochem Mol Biol 31:1–5

    Article  CAS  PubMed  Google Scholar 

  22. Jones AME, Winge P, Bones AM, Cole R, Rossiter JT (2002) Characterization and evolution of a myrosinase from the cabbage aphid Brevicoryne brassicae. Insect Biochem Mol Biol 32:275–284

    Article  CAS  PubMed  Google Scholar 

  23. Kuchernig JC, Burow M, Wittstock U (2012) Evolution of specifier proteins in glucosinolate-containing plants. BMC Evol Biol 12:127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lu M, Hashimoto K, Uda Y (2011) Rat intestinal microbiota digest desulfosinigrin to form allyl cyanide and 1-cyano-2,3-epithiopropane. Food Res Int 44:1023–1028

    Article  CAS  Google Scholar 

  25. Luang-In V, Rossiter JT (2015) Stability studies of isothiocyanates and nitriles in aqueous media. Songklanakarin J Sci Technol 37:625–630

    Google Scholar 

  26. Luang-In V, Narbad A, Nueno-Palop C, Mithen R, Bennett M, Rossiter JT (2014) The metabolism of methylsulfinylalkyl- and methylthioalkyl-glucosinolates by a selection of human gut bacteria. Mol Nutr Food Res 58:875–883

    Article  CAS  PubMed  Google Scholar 

  27. Luciano FB, Holley RA (2011) Bacterial degradation of glucosinolates and its influence on the growth of E. coli 0157:H7. Fleischwirtsch Int 1:78–81

    Google Scholar 

  28. Macleod AJ, Rossiter JT (1985) The occurrence and activity of epithiospecifier protein in some cruciferae seeds. Phytochemistry 24:1895–1898

    Article  CAS  Google Scholar 

  29. Macleod AJ, Rossiter JT (1987) Degradation of 2-hydroxybut-3-enylglucosinolate (progoitrin). Phytochemistry 26:669–673

    Article  CAS  Google Scholar 

  30. Matusheski NV, Jeffery EH (2001) Comparison of the bioactivity of two glucoraphanin hydrolysis products found in broccoli, sulforaphane and sulforaphane nitrile. J Agric Food Chem 49:5743–5749

    Article  CAS  PubMed  Google Scholar 

  31. Mays JR, Roska RLW, Sarfaraz S, Mukhtar H, Rajski SR (2008) Identification, synthesis, and enzymology of non-natural glucosinolate chemopreventive candidates. ChemBioChem 9:729–747

    Article  CAS  PubMed  Google Scholar 

  32. Mullaney JA, Kelly WJ, McGhie TK, Ansell J, Heyes JA (2013) Lactic acid bacteria convert glucosinolates to nitriles efficiently yet differently from Enterobacteriaceae. J Agric Food Chem 61:3039–3046

    Article  CAS  PubMed  Google Scholar 

  33. Nallasamy P, Si H, Babu PVA, Pan D, Fu Y, Brooke EAS, Shah H, Zhen W, Zhu H, Liu D, Li Y, Jia Z (2014) Sulforaphane reduces vascular inflammation in mice and prevents TNF-alpha-induced monocyte adhesion to primary endothelial cells through interfering with the NF-kappa B pathway. J Nutr Biochem 25:824–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nho CW, Jeffery E (2001) The synergistic upregulation of phase II detoxification enzymes by glucosinolate breakdown products in cruciferous vegetables. Toxicol Appl Pharmacol 174:146–152

    Article  CAS  PubMed  Google Scholar 

  35. Palop ML, Smiths JP, Tenbrink B (1995) Degradation of sinigrin by Lactobacillus agilis strain r16. Int J Food Microbiol 26:219–229

    Article  CAS  Google Scholar 

  36. Rask L, Andreasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol 42:93–113

    Article  CAS  PubMed  Google Scholar 

  37. Shehatou GSG, Suddek GM (2016) Sulforaphane attenuates the development of atherosclerosis and improves endothelial dysfunction in hypercholesterolemic rabbits. Exp Biol Med 241:426–436

    Article  CAS  Google Scholar 

  38. Smits JP, Knol W, Bol J (1993) Glucosinolate degradation by Aspergillus clavatus and Fusarium oxysporum in liquid and solid-state fermentation. Appl Microbiol Biotechnol 38:696–701

    Article  CAS  Google Scholar 

  39. Spencer GF, Daxenbichler ME (1980) Gas chromatography–mass spectrometry of nitriles, isothiocyanates and oxazolidinethiones derived from cruciferous glucosinolates. J Sci Food Agric 31:359–367

    Article  CAS  Google Scholar 

  40. Sun C, Yang C, Xue R, Li S, Zhang T, Pan L, Ma X, Wang L, Li D (2015) Sulforaphane alleviates muscular dystrophy in mdx mice by activation of Nrf2. J Appl Physiol 118:224–237

    Article  PubMed  Google Scholar 

  41. Tani N, Ohtsuru M, Hata T (1974) Studies on bacterial myrosinase. 1. Isolation of myrosinase producing microorganism. Agric Biol Chem 38:1617–1622

    CAS  Google Scholar 

  42. Tanil H, Higashi T, Nishimura F, Higuchi Y, Saijoh K (2008) Effects of cruciferous allyl nitrile on phase 2 antioxidant and detoxification enzymes. Med Sci Monit 14:BR189–BR192

    Google Scholar 

  43. Thies W (1988) Isolation of sinigrin and glucotropaeolin from cruciferous seeds. Fett Wiss Technol Fat Sci Technol 90:311–314

    CAS  Google Scholar 

  44. Tian G, Tang P, Xie R, Cheng L, Yuan Q, Hu J (2016) The stability and degradation mechanism of sulforaphene in solvents. Food Chem 199:301–306

    Article  CAS  PubMed  Google Scholar 

  45. Traka M, Mithen R (2009) Glucosinolates, isothiocyanates and human health. Phytochem Rev 8:269–282

    Article  CAS  Google Scholar 

  46. Traka MH, Mithen RF (2011) Plant science and human nutrition: challenges in assessing health-promoting properties of phytochemicals. Plant Cell 23:2483–2497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Traka MH, Melchini A, Mithen RF (2014) Sulforaphane and prostate cancer interception. Drug Discov Today 19:1488–1492

    Article  CAS  PubMed  Google Scholar 

  48. Uda Y, Kurata T, Arakawa N (1986) Effects of ph and ferrous ion on the degradation of glucosinolates by myrosinase. Agric Biol Chem 50:2735–2740

    CAS  Google Scholar 

  49. Wathelet JP, Iori R, Leoni O, Rollin P, Mabon N, Marlier M, Palmieri S (2001) A recombinant beta-O-glucosidase from Caldocellum saccharolyticum to hydrolyse desulfo-glucosinolates. Biotechnol Lett 23:443–446

    Article  CAS  Google Scholar 

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Acknowledgments

The authors wish to acknowledge the Royal Thai Government for Scholarship awarded to VL and the UK Biotechnology and Biological Sciences Research Council (BB/J004545/1) for partial financial support of this research.

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  1. Vijitra Luang-In

    Present address: Natural Antioxidant Research Unit, Department of Biotechnology, Faculty of Technology, Mahasarakham University, Khamriang, Kantarawichai, Mahasarakham, 44150, Thailand

Authors and Affiliations

  1. Faculty of Life Sciences, Imperial College London, Exhibition Rd, London, SW7 2AZ, UK

    Vijitra Luang-In, Abdulhadi Ali Albaser, Mark H. Bennett & John T. Rossiter

  2. Microbiology Section, Department of Plant Science, Faculty of Science, University of Sebha, PO Box 18758, Sebha, Libya

    Abdulhadi Ali Albaser

  3. Gut Health and Food Safety Programme, Institute of Food Research, Colney Lane, Norwich, NR4 7UA, UK

    Carmen Nueno-Palop & Arjan Narbad

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  1. Vijitra Luang-In
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Correspondence to Vijitra Luang-In.

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Luang-In, V., Albaser, A.A., Nueno-Palop, C. et al. Glucosinolate and Desulfo-glucosinolate Metabolism by a Selection of Human Gut Bacteria. Curr Microbiol 73, 442–451 (2016). https://doi.org/10.1007/s00284-016-1079-8

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  • DOI: https://doi.org/10.1007/s00284-016-1079-8

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