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Characterization of vitamin B12 compounds from marine foods

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  • Chemistry and Biochmistry
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Abstract

Vitamin B12 is synthesized by only certain bacteria and archaea but not by animals or plants. In marine environments, bacterial vitamin B12 is transferred and concentrated into fish and shellfish bodies by plankton in the marine food chain. Moreover, marine macrophytic red algae, Porphyra spp. specifically contain substantial amounts of vitamin B12, due to microbial interaction. Although some meats or viscera of edible fish and shellfish are excellent sources of biologically active vitamin B12, an inactive corrinoid, pseudovitamin B12, was found in some edible shellfish using liquid chromatography/electrospray ionization–tandem mass spectrometry. To prevent elderly people from developing vitamin B12 deficiency due to food protein-bound vitamin B12 malabsorption, we present a survey of marine foods containing free vitamin B12. The results of our study suggest that bonito and clam extracts (or soup stocks), which contain considerable amounts of free vitamin B12 are useful not only as seasonings and flavorings but also as excellent sources of free vitamin B12.

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References

  • Adachi S, Miyamoto E, Watanabe F, Enomoto E, Kuda T, Hayashi M, Nakano Y (2005) Purification and characterization of a corrinoid compound from a Japanese salted and fermented salmon kidney “Mefun”. J Liq Chrom Rel Technol 28:2561–2569

    Article  CAS  Google Scholar 

  • Andrès E, Affenberger S, Vinzio S, Kurtz JE, Noel E, Kaltenbach G, Maloisel F, Shlienger JL, Blicklè JF (2005) Food-cobalamin malabsorption in elderly patients: clinical manifestations and treatment. Am J Med 118:1154–1159

    Article  PubMed  CAS  Google Scholar 

  • Angyal G (1996) In: Methods for the microbiological analysis of selected nutrients. AOAC international, MD, 63–65

  • Bertrand EM, McCrow JP, Moustafa A, Zheng H, McQuaid JM, Delmont TO, Post AF, Sipler RE, Spackeen JL, Xu K, Bronk DA, Hutchins D (2015) Phytoplankton-bacterial interactions mediated micronutrient colimitation at the coastal Antarctic Sea ice edge. Proc Natl Acad Sci USA 112:9938–9943

    Article  PubMed  CAS  Google Scholar 

  • Bito T, Teng F, Ohishi N, Takenaka S, Miyamoto E, Sakuno E, Terashima K, Yabuta Y, Watanabe F (2014) Characterization of vitamin B12 compounds in the fruiting bodies of shiitake mushroom (Lentinula edodes) and bed logs after fruiting of the mushroom. Mycoscience 55:464–468

    Article  CAS  Google Scholar 

  • Bito T, Bito M, Asai Y, Takenaka S, Yabuta Y, Tago K, Ohnishi M, Mizoguchi T, Watanabe F (2016) Characterization and quantitation of vitamin B12 compounds in various Chlorella supplements. J Agric Food Chem 64:8516–8524

    Article  PubMed  CAS  Google Scholar 

  • Bito T, Teng F, Watanabe F (2017) Bioactive compounds of edible purple laver Porphyra sp. (Nori). J Agric Food Chem 65:10685–10692

    Article  PubMed  CAS  Google Scholar 

  • Bourre JME, Paquotte PM (2008) Contribution (in 2005) of marine and fresh water products (finfish and shellfish, seafood, wild and formed) to the French dietary intakes of vitamin D and B12, selenium, iodine and docosahexaenoic acid: impact on public health. Int J Food Nutr 59:491–501

    Article  CAS  Google Scholar 

  • Brouwer-Brolsma EM, Dhonukshe-Rutten RAM, van Wijngaarden JP, van der Zwaluw NL, van der Velde N, de Groot LCPGM (2015) Dietary sources of vitamin B12 and their association with vitamin B12 status markers in healthy older adults in the B-PROOF study. Nutrients 7:7781–7797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Z, Crippen K, Gulati S, Banerjee R (1994) Purification and kinetic mechanism of a mammalian methionine synthase from pig liver. J Biol Chem 269:27193–27197

    PubMed  CAS  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93

    Article  PubMed  CAS  Google Scholar 

  • Doxey AC, Kurtz DA, Lynch MDJ, Sauder LA, Neufeld JD (2015) Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production. ISME J 9:461–471

    Article  PubMed  CAS  Google Scholar 

  • Farquharson J, Adams JF (1976) The forms of vitamin B12 in foods. Br J Nutr 36:127–136

    Article  PubMed  CAS  Google Scholar 

  • Fenton WA, Hack AM, Willard HF, Gertler A, Rosenberg LE (1982) Purification and properties of methylmalonyl coenzyme A mutase from human liver. Arch Biochem 228:323–329

    Google Scholar 

  • Green R, Allen LH, Bjørke-Monsen AL, Brito A, Guéant JW, Molloy AM, Nexo E, Stabler S, Toh BH, Ueland PM, Yainik C (2017) Vitamin B12 deficiency. Nat Rev Dis Primers 3:17040

    Article  PubMed  Google Scholar 

  • Grienke U, Silke J, Tasdemir D (2014) Bioactive compounds from marine mussels and their effects on human health. Food Chem 142:48–60

    Article  PubMed  CAS  Google Scholar 

  • Heal KR, Carlson LT, Devol AH, Armbrust EV, Moffett JM, Stahl DA, Ingalls AE (2014) Determination of four forms of vitamin B12 and other B vitamins in seawater by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 28:2398–2404

    Article  PubMed  CAS  Google Scholar 

  • Heal KR, Qin W, Ribalet F, Bertagnolli AD, Coyote-Maestas W, Hmelo LR, Moffett JW, Devol AH, Armbrust EV, Stahl DA, Ingalls AE (2017) Two distinct pools of B12 analogs reveal community interdependencies in the ocean. Proc Natl Acad Sci USA 114:364–369

    Article  PubMed  CAS  Google Scholar 

  • Helliwell KE (2017) The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol 216:62–68

    Article  PubMed  CAS  Google Scholar 

  • Helliwell KE, Lawrence AD, Holzer A, Kudahl UJ, Sasso S, Kräutler B, Scanlan DJ, Warren MJ, Smith AG (2016) Cyanobacteria and eukaryotic algae use different chemical variants of vitamin B12. Cur Biol 26:999–1008

    Article  CAS  Google Scholar 

  • Herbert V. (1996) Vitamin B12. In: Present knowledge in nutrition, 7th ed. Filer LJ, Ziegler E (eds) Washington DC, International Life Science Institute Press, 191–205

  • Iguchi H, Yurimoto H, Sakai Y (2015) Interactions of methylotrophs with plants and other heterotrophic bacteria. Microorganims 3:137–151

    Article  CAS  Google Scholar 

  • Ishihara Y, Imai E, Takenaka S, Fujita T, Yabuta Y, Masuda S, Watanabe F (2011) Characterization of a corrinoid compound from pacific bluefin tuna (Thunnus orientalis) liver. Food Sci Technol Res 17:589–594

    Article  CAS  Google Scholar 

  • Institute of Medicine. Vitamin B12 (1998) In: Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, biotin, and choline; Institute of Medicine, National Academy Press: Washington, DC, USA, 306–356

  • Ishihara Y, Miyamoto E, Takenaka S, Yabuta Y, Watanabe F (2012) Characterization of vitamin B12 compound from Japanese common squid liver. Nippon Suisan Gakkaishi 78:749–751 (in Japanese with English abstract)

    Article  CAS  Google Scholar 

  • Ishihara Y, Ueta K, Bito T, Takenaka S, Yabuta Y, Watanabe F (2013) Characterization of vitamin B12 compounds from the brackish-water bivalve Corbicula japonica. Fish Sci 79:321–326

    Article  CAS  Google Scholar 

  • Juzeniene A, Nizauskaite Z (2013) Photodegradation of cobalamins in aqueous solutions and in human blood. J Photochem Photobiol B: Biol 122:7–14

    Article  CAS  Google Scholar 

  • Keller S, Ruetz M, Kunze C, Krautler B, Diekert G, Schubert T (2014) Exogenous 5,6-dimethylbenzimidazole caused production of a non-functional tetrachloroethene reductive dehalogenase in Sulfurospirillum multivorans. Environ Microbiol 16:3361–3369

    Article  PubMed  CAS  Google Scholar 

  • Lafarga T, Hayes M (2014) Bioactive peptides from meat muscle and by-products: generation, functionality and application as functional ingredients. Meat Sci 98:227–239

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Shin JH, Park JM, Kim HJ, Ahn JH, Kwak BM, Kim JM (2015) Analytical determination of vitamin B12 content in infant and toddler milk formulas by liquid chromatography tandem mass spectrometry (LC-MS/MS). Korean J Food Sci An 35:765–771

    Article  Google Scholar 

  • Limsuwan T, Lovell RT (1981) Intestinal synthesis and absorption of vitamin B12 in channel catfish. J Nutr 111:2125–2132

    Article  PubMed  CAS  Google Scholar 

  • Millet P, Guilland JC, Fuchs F, Klepping J (1989) Nutrient intake and vitamin status of healthy French vegetarians and nonvegetarians. Am J Clin Nutr 50:718–727

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto E, Tanioka Y, Nakao T, Barla F, Inui H, Fujita T, Watanabe F, Nakano Y (2006) Purification and characterization of a corrinoid compound in an edible cyanobacterium Aphanizomenon flos-aquae as a nutritional supplementary food. J Agric Food Chem 54:9604–9607

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto E, Yabuta Y, Kwak CS, Enomoto T, Watanabe F (2009) Characterization of vitamin B12 compounds from Korean purple laver (Porphyra sp.) products. J Agric Food Chem 57:2793–2796

    Article  PubMed  CAS  Google Scholar 

  • Nishioka M, Kanosue F, Tanioka Y, Miyamoto E, Watanabe F (2006) Characterization of vitamin B12 in skipjack tuna meats and loss of the vitamin from the fish meats by various cooking conditions. Vitamins 80:507–511

    CAS  Google Scholar 

  • Nishioka M, Tanioka Y, Miyamoto E, Enomoto T, Watanabe F (2007) TLC analysis of a corrinoid compound from dark muscle of the yellowfin tuna (Thunnus albacares). J Liq Chrom Rel Technol 30:2245–2252

    Article  CAS  Google Scholar 

  • Nishioka M, Kanosue F, Miyamoto E, Yabuta Y, Watanabe F (2008) Bonito extract as a natural and excellent source of free vitamin B12. Curr Top Nutr Res 6:105–108

    Google Scholar 

  • Nishioka M, Kanosue F, Miyamoto E, Yabuta Y, Watanabe F (2009) TLC-bioautogram analysis of vitamin B12 compounds from boiled and dried Japanese anchovy (Engraulis japonica) products. J Liq Chrom Rel Technol 32:1175–1182

    Article  CAS  Google Scholar 

  • Nishioka M, Kanosue F, Yabuta Y, Watanabe F (2010) Vitamin B12 contents of skipjack tuna meats and internal organs. Vitamins 84:322–324

    CAS  Google Scholar 

  • Nishioka M, Kanosue F, Yabuta Y, Watanabe F (2011) Loss of vitamin B12 in fish (round herring) meats during various cooking treatments. J Nutr Sci Vitaminol 57:432–436

    Article  PubMed  CAS  Google Scholar 

  • Pietra F (2015) Uptake of organohalide pollutants, and release of partially dehalogenated products, by NpRdhA, a ‘base-off’ cob(II)alamin-dependent reductive dehalogenase from a deep sea bacterium. A molecular dynamics investigation. Chem Biodiv 12:1945–1953

    Article  CAS  Google Scholar 

  • Sañudo-Wilhelmy SA, Cutter LS, Durazo R, Smail EA, Gómez-Consarnau L, Webb EA, Prokopenko MG, Berelson WM, Karl DM (2012) Multiple B-vitamin depletion in large areas of the coastal ocean. Proc Natl Acad Sci USA 109:14041–14045

    Article  PubMed  Google Scholar 

  • Scheers N, Lindqvist H, Langkilde AM, Undeland I, Sandberg AS (2014) Vitamin B12 as a potential compliance marker for fish intake. Eur J Nutr 53:1327–1333

    Article  PubMed  CAS  Google Scholar 

  • Scheider Z, Stroiñski A (1987) Biosynthesis of vitamin B12. In: Scheider Z et al (eds) Comprehensive B12. Walter de Gruyter, Germany, pp 93–110

    Chapter  Google Scholar 

  • Shibata K, Fukuwatari T, Imai E, Hayakawa T, Watanabe F, Takimoto H, Watanabe T, Umegaki K (2013) Dietary reference intakes for Japanese 2010: water-soluble vitamins. J Nutr Sci Vitaminol 59:S67–S82

    Article  CAS  Google Scholar 

  • Stadnik J, Keska P (2015) Meat and fermented meat products as a source of bioactive peptides. Acta Sci Pol Technol Aliment 14:181–190

    Article  PubMed  CAS  Google Scholar 

  • Standard Tables of Food Composition in Japan-2010 (2010) The Council for Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, Japan. Tokyo, Official gazette co-operation of Japan

  • Takenaka S, Sugiyama S, Ebara S, Miyamoto E, Abe K, Tamura Y, Watanabe F, Tsuyama S, Nakano Y (2001) Feeding dried purple laver (nori) to vitamin B12-deficient rats significantly improves vitamin B12 status. Br J Nutr 85:699–703

    Article  PubMed  CAS  Google Scholar 

  • Takenaka S, Enomoto T, Tsuyama S, Watanabe F (2003) TLC analysis of corrinoid compounds in fish sauce. J Liq Chrom Rel Technol 26:2703–2707

    Article  CAS  Google Scholar 

  • Tanioka Y, Yabuta Y, Miyamoto E, Inui H, Watanabe F (2008) Analysis of vitamin B12 in food by silica gel 60 TLC and bioautography with vitamin B12-dependent Escherichia coli 215. J Liq Chrom Rel Technol 31:1977–1985

    Article  CAS  Google Scholar 

  • Tanioka Y, Miyamoto E, Yabuta Y, Ohnishi K, Fujita T, Yamaji R, Misono H, Shigeoka S, Nakano Y, Inui H, Watanabe F (2010) Methyladeninylcobamide functions as the cofactor of methionine synthase in a cyanobacterium, Spirulina platensis NIES-39. FEBS Lett 584:3223–3226

    Article  PubMed  CAS  Google Scholar 

  • Tanioka Y, Takenaka S, Furusho T, Yabuta Y, Nakano Y, Watanabe F (2012) Characterization of vitamin B12-related compounds isolated from edible portion of abalone. Vitamins 86:390–394

    CAS  Google Scholar 

  • Tanioka Y, Takenaka S, Furusho T, Yabuta Y, Nakano Y, Watanabe F (2014) Identification of vitamin B12 and pseudovitamin B12 from various edible shellfish using liquid chromatography-electrospray ionization/tandem mass spectrometry. Fish Sci 80:1065–1071

    Article  CAS  Google Scholar 

  • Teng F, Bito T, Takenaka S, Yabuta Y, Watanabe F (2014) Vitamin B12[c-lactone], a biologically inactive corrinoid compound, occurs in cultured and dried lion’s mane mushroom (Hericium erinaceus) fruiting bodies. J Agric Food Chem 62:1726–1732

    Article  PubMed  CAS  Google Scholar 

  • Teng F, Tanioka Y, Hamaguchi N, Bito T, Takenaka S, Yabuta Y, Watanabe F (2015a) Determination and characterization of vitamin B12 compounds in edible sea snails, ivory shell Babylonia japonica and turban shell Turdo Batillus cornutus. Fish Sci 81:1105–1111

    Article  CAS  Google Scholar 

  • Teng F, Tanioka Y, Bito T, Takenaka S, Yabuta Y, Watanabe F (2015b) Occurrence of biologically inactive corrinoid compounds in canned edible apple snail (escargots). Food Nutr Sci 6:1071–1077

    CAS  Google Scholar 

  • Teng F, Tanioka Y, Hamaguchi N, Bito T, Takenaka S, Yabuta Y, Watanabe F (2015c) Determination and characterization of vitamin B12 compounds in edible sea snails, ivory shell Babylonia japonica and turban shell Turdo Batillus cornutus. Fish Sci 81:1105–1111

    Article  CAS  Google Scholar 

  • Teng F, Bito T, Takenaka S, Yabuta Y, Watanabe F (2016) Yolk of the century egg (pidan) contains a readily digestible form of free vitamin B12. J Nutr Sci Vitaminol 62:366–371

    Article  PubMed  CAS  Google Scholar 

  • Ueta K, Nishioka M, Yabuta Y, Watanabe F (2010) TLC-bioautography analysis of vitamin B12 compound from the short-necked clam (Ruditapes philippinarum) extract used as a flavoring. J Liq Chrom Rel Technol 33:972–979

    Article  CAS  Google Scholar 

  • Ueta K, Ishihara Y, Yabuta Y, Masuda S, Watanabe F (2011a) TLC-analysis of a corrinoid compound from Japanese rock-oyster “iwa-gaki” (Crassostrea nippona). J Liq Chrom Rel Technol 34:928–935

    Article  CAS  Google Scholar 

  • Ueta K, Takenaka S, Yabuta Y, Watanabe F (2011b) Broth from canned clams is suitable for use as an excellent source of free vitamin B12. J Agric Food Chem 59:12054–12058

    Article  PubMed  CAS  Google Scholar 

  • Vogiatzoglou A, Smith AD, Nurk E, Berstad P, Crevon CA, Ueland PM, Vollset SE, Tell GS, Refsum H (2009) Dietary sources of vitamin B12 and their association with plasma vitamin B12 concentrations in the general population: the Hordaland Homocyteine Study. Am J Clin Nutr 89:1078–1097

    Article  PubMed  CAS  Google Scholar 

  • Watanabe F, Bito T (2016) Corrinoids in food and biological samples. In: Atta-ur-Rahman (ed) Frontiers in natural product chemistry. Bentham Science Publishers, Sharjah, pp 229–244

  • Watanabe F, Bito T (2018) Vitamin B12 sources and microbial interaction. Exp Biol Med 243:148–158

    Article  CAS  Google Scholar 

  • Watanabe F, Miyamoto E (2003) Hydrophilic vitamins. In: Handbook of thin-layer chromatography, 3rd ed. revised and expanded. Marcel Dekker, New York, pp 589 − 605

  • Watanabe F, Takenaka S, Katsura H, Masumder SAMZH, Abe K, Tamura Y, Nakano Y (1999a) Dried green and purple lavers (nori) contain substantial amounts of biologically active vitamin B12 but less of dietary iodine relative to other edible seaweeds. J Agric Food Chem 47:2341–2343

    Article  PubMed  CAS  Google Scholar 

  • Watanabe F, Katsura H, Takenaka S, Fujita T, Abe K, Tamura Y, Nakatsuka T, Nakano Y (1999b) Pseudovitamin B12 is the predominate cobamide of an algal health food, spirulina tablets. J Agric Food Chem 47:4736–4741

    Article  PubMed  CAS  Google Scholar 

  • Watanabe F, Takenaka S, Katsura H, Miyamoto E, Abe K, Tamura Y, Nakatsuka T, Nakano Y (2000) Characterization of a vitamin B12 compound in the edible purple laver, Porphyra yesoensis. Biosci Biotechnol Biochem 64:2712–2715

    Article  PubMed  CAS  Google Scholar 

  • Watanabe F, Katsura H, Takenaka S, Enomoto T, Miyamoto E, Nakatsuka T, Nakano Y (2001) Characterization of vitamin B12 compounds from edible shellfish, clam, oyster, and mussel. Int J Food Sci Nutr 52:263–268

    Article  PubMed  CAS  Google Scholar 

  • Watanabe F, Takenaka S, Kittaka-Katsura H, Ebara S, Miyamoto E (2002) Characterization and bioavailability of vitamin B12-compounds from edible algae. J Nutr Sci Vitaminol 48:325–331

    Article  PubMed  CAS  Google Scholar 

  • Watanabe F, Michihata T, Takenaka S, Kittaka-Katsura H, Enomoto T, Miyamoto E, Adachi S (2004) Purification and characterization of corrinoid compounds from a Japanese fish sauce. J Liq Chrom Rel Technol 27:2113–2119

    Article  CAS  Google Scholar 

  • Watanabe F, Schwarz J, Takenaka S, Miyamoto E, Ohishi N, Nelle E, Hochstrasser R, Yabuta Y (2013) Characterization of vitamin B12 compounds in the wild edible mushrooms black trumpet (Craterellus cornucopioides) and golden chanterelle (Cantharellus cibarius). J Nutr Sci Vitaminol 58:50–53

    Google Scholar 

  • Watanabe F, Yabuta Y, Bito T. (2014a) Tetrapyrrole compounds of cyanobacteria. In: Atta-ur-Rahman (ed) Studies in natural products chemistry. Elsevier Science Publishers, Amsterdam, pp 341–349

  • Watanabe F, Yabuta Y, Bito T, Teng F (2014b) Vitamin B12-containing plant food sources for vegetarians. Nutrients 6:1861–1873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamada S, Sasa M, Yamada K, Fukuda M (1996) Release and uptake of vitamin B12 by Asakusanori (Porphyra tenera) seaweed. J Nutr Sci Vitaminol 42:507–515

    Article  PubMed  CAS  Google Scholar 

  • Yoshino K, Inagawa M, Oshima M, Yokota K, Umesawa M, Endo M, Yamagashi K, Tanigawa T, Sato S, Shimamoto T, Iso H (2005) Trends in dietary intake of folate, vitamin B6 and vitamin B12 among Japanese adults in two rural communities from 1971 through 2001. J Epidemiol 15:29–37

    Article  PubMed  Google Scholar 

  • Zironi E, Gassotti T, Barbarossa A, Devicienti C, Scardilli M, Pagliuca G (2013) Technical note: development and validation of a method using ultra performance liquid chromatography coupled with tandem mass spectrometry for determination of vitamin B-12 concentration in milk and dairy products. J Dairy Res 96:2832–2836

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported in part by JSPS KAKENHI (25450168 to F.W. and 24700856 to Y.T.).

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Correspondence to Fumio Watanabe.

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Bito, T., Tanioka, Y. & Watanabe, F. Characterization of vitamin B12 compounds from marine foods. Fish Sci 84, 747–755 (2018). https://doi.org/10.1007/s12562-018-1222-5

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