Vitamin B12 is synthesized only by certain bacteria and archaeon, but not by plants. The synthesized vitamin B12 is transferred and accumulates in animal tissues, which can occur in certain plant and mushroom species through microbial interaction. In particular, the meat and milk of herbivorous ruminant animals (e.g. cattle and sheep) are good sources of vitamin B12 for humans. Ruminants acquire vitamin B12, which is considered an essential nutrient, through a symbiotic relationship with the bacteria present in their stomachs. In aquatic environments, most phytoplankton acquire vitamin B12 through a symbiotic relationship with bacteria, and they become food for larval fish and bivalves. Edible plants and mushrooms rarely contain a considerable amount of vitamin B12, mainly due to concomitant bacteria in soil and/or their aerial surfaces. Thus, humans acquire vitamin B12 formed by microbial interaction via mainly ruminants and fish (or shellfish) as food sources. In this review, up-to-date information on vitamin B12 sources and bioavailability are also discussed.
Impact statement
To prevent vitamin B12 (B12) deficiency in high-risk populations such as vegetarians and elderly subjects, it is necessary to identify foods that contain high levels of B12. B12 is synthesized by only certain bacteria and archaeon, but not by plants or animals. The synthesized B12 is transferred and accumulated in animal tissues, even in certain plant tissues via microbial interaction. Meats and milks of herbivorous ruminant animals are good sources of B12 for humans. Ruminants acquire the essential B12 through a symbiotic relationship with bacteria inside the body. Thus, we also depend on B12-producing bacteria located in ruminant stomachs. While edible plants and mushrooms rarely contain a considerable amount of B12, mainly due to concomitant bacteria in soil and/or their aerial surfaces. In this mini-review, we described up-to-date information on B12 sources and bioavailability with reference to the interaction of microbes as B12-producers.
WatanabeFMiyamotoE. Hydrophilic vitamins. In: Sherma J, Fried B (eds) Handbook of thin-layer chromatography, 3rd ed. revised and expanded. New York: Dekker, 2003, pp.589 − 605
2.
ChenZCrippenKGulatiSBanerjeeR.Purification and kinetic mechanism of a mammalian methionine synthase from pig liver. J Biol Chem1994;
269:27193−7
3.
FentonWAHackAMWillardHFGertlerARosenbergLE.Purification and properties of methylmalonyl coenzyme A mutase from human liver. Arch Biochem1982;
228:323–9
4.
ScheiderZStroiñskiA.Biosynthesis of vitamin B12. In: ScheiderZStroiñskiA (eds) Comprehensive B12.
Germany:
de Gruyter, 1987, pp.93 − 110
5.
HeldtDLawrenceADLindenmeyerMDeeryEHeathcotePRigbySEWarrenMJ.Aerobic synthesis of vitamin B12: ring contraction and cobalt chelation. Biochem Soc Trans2005;
33:815–9
6.
MooreSJWarrenMJ.The anaerobic biosynthesis of vitamin B12. Biochem Soc Trans2012;
40:581–6
7.
RenzP.Biosynthesis of the 5,6-demethylbenzimidazole moiety of cobalamin and of the other bases found in natural corrinoids. In: BanerjeeR (ed.) Chemistry and biochemistry of B12.
New York:
John-Wiley & Sons Inc., 1999, pp.557–75
8.
WatanabeFBitoT.Corrinoids in food and biological samples. In: RahmanA (ed.) Frontiers in natural product chemistry (
vol.2).
Sharjah:
Bentham Science Publishers, 2016, pp.229–44
9.
TengFTaniokaYBitoTTakenakaSYabutaYWatanabeF.Occurrence of biologically inactive corrinoid compounds in canned edible apple snail (escargots). Food Nutr Sci2015;
6:1071–7
10.
WatanabeF.Vitamin B12 sources and bioavailability. Exp Biol Med (Maywood)2007;
232:1266–74
11.
Brouwer-BrolsmaEMDhonukshe-RuttenRAMvan WijngaardenJPvan der ZwaluwNLvan der VeldeNde GrootLCPGM.Dietary sources of vitamin B12 and their association with vitamin B12 status markers in healthy older adults in the B-PROOF study. Nutrients2015;
7:7781–97
12.
TuckerKLRichSRosenbergIJacquesPDallalGWilsonPWSelhubJ.Plasma vitamin B12 concentrations relate to intake source in the Framingham Offspring study. Am J Clin Nutr2000;
71:514–22
13.
VogiatzoglouASmithADNurkEBerstadPCrevonCAUelandPMVollsetSETellGSRefsumH.Dietary sources of vitamin B12 and their association with plasma vitamin B12 concentrations in the general population: the Hordaland Homocyteine Study. Am J Clin Nutr2009;
89:1078–97
14.
SmithSELoosliJK.Cobalt and vitamin B12 in ruminant nutrition: a review. J Dairy Sci1957;
40:1215–27
15.
Ortigues-MartyIMicolDPracheSDoziasDGirardCL.Nutritional value of meat: the influence of nutrition and physical activity on vitamin B12 concentrations in ruminant tissues. Reprod Nutr Dev2005;
45:453–67
16.
KawashimaTHenryPRAmmermanCBLittellRC.Bioavailability of cobalt sources for ruminants. 2. Estimation of the relative value of reagent grade and feed grade cobalt sources from tissue cobalt accumulation and vitamin B12 concentrations. Nutr Res1997;
17:957–74
17.
StanglGISchwarzFJJahnBKirchgessnerM.Cobalt-deficiency-induced hyperhomocysteineaemia and oxidative status of cattle. Br J Nutr2000;
83:3–6
18.
TiffanyMEFellnerVSpearsJW.Influence of cobalt concentration on vitamin B12 production and fermentation of mixed ruminal microorganisms grown in continuous culture flow-through fermentors. J Anim Sci2006;
84:635–40
19.
KincaidRLLefebveLECronrathJDSochaMTJohnsonAB.Effect of dietary cobalt supplementation on cobalt metabolism and performance of dairy cattle. J Dairy Sci2003;
86:1405–14
20.
BishehsariSTabatabaeiMMAliarabiHAlipourDZamaniPAhmadiA.Effect of dietary cobalt supplementation on plasma and rumen metabolites in Mehraban lambs. Small Ruminant Res2010;
90:170–3
21.
Standard Tables of Food Composition in Japan – 2010. The Council for Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, Japan. Tokyo: Official Gazette Co-operation of Japan, 2010.
22.
Al-FataftahARAHerzallahSMAlshawabkehKIbrahimSA.Administration of lactic acid bacteria to enhance synthesis of vitamin B12 and B6 and lower cholesterol levels in poultry meat. J Food Agric Environ2013;
11:604–9
23.
GilleDSchmidA.Vitamin B12 in meat and dairy products. Nutr Rev2015;
73:106–15
24.
Ortigues-MartyIThomasEPrévéraudDPGirardCLBauchartDDurandDPeyronA.Influence of maturation and cooking treatments on the nutritional value of bovine meats: water losses and vitamin B12. Meat Sci2006;
73:451–8
25.
KojimaAOzekiANakanishiTSatoYChibaTAbeKUmegakiK.Literature review on vitamin loss from foods during cooking (part 1) – fat soluble vitamins, and vitamin B1, B2, B6 and B12. Vitamins (in Japanese)2017;
91:1–27
26.
CreedPG.The sensory and nutritional quality of ‘sous vide’ foods. Food Control1995;
6:45–52
27.
Raynal-LjutovacKLagriffoulGPaccardPGuilletIChilliardY.Composition of goat and sheep milk products: an update. Small Ruminant Res2008;
79:57–72
28.
MatteJBrittenMGirardCL.The importance of milk as a source of vitamin B12 for human nutrition. Anim Front2014;
4:32–7
29.
MillerJWentworthJMcCulloghME.Effects of various factors on vitamin B12 content of cow’s milk. J Agric Food Chem1966;
14:218–21
30.
DuplessisMPellerinDCueRIGirardCL.Factors affecting vitamin B12 concentration in milk of commercial dairy herds: an exploratory study. J Dairy Sci2016;
99:4886–92
31.
RuttenMJMBouwmanACSprongRCvan ArendonkJAMViskerMHPW.Genetic variation in vitamin B12 content of bovine milk and its association with SNP along the bovine genome. Plos One2013;
8:e62382
32.
FedosovSNPetersenTENexøE.Transcobalamin from cow milk: isolation and physico-chemical properties. Biochim Biophys Acta1996;
292:113–9
33.
BurgerRLAllenRH.Characterization of vitamin B12-binding proteins isolated from human milk and saliva by affinity chromatography. J Biol Chem1974;
249:7220–7
34.
MatteJJGuayFGiardCL.Bioavailability of vitamin B12 in cow’s milk. Br J Nutr2012;
107:61–6
35.
BitoTTanabeTTaniokaYTakenakaSYabutaYWatanabeF.Determination of vitamin B12 content in 26 types of natural cheeses and identification of vitamin B12 compounds in those cheeses. Vitamins (in Japanese)2016;
90:390–4
36.
JohnsPWDasAKuilESJacobsWASchimpfKJSchmitzDJ.Cocoa polyphenols accelerate vitamin B12 degradation in heated chocolate milk. Int J Food Sci Technol2015;
50:421–30
37.
AllenCParksOW.Photodegradation of riboflavin in milks exposed to fluorescent light. J Dairy Sci1979;
62:1377–9
38.
TobaTAdachiSAraiI.Sunlight and sodium hypochloride induced color changes in milk. J Dairy Sci1980;
63:1796–801
39.
Kra¨UtlerBStepanekR.Photooxygenolysis of vitamin B12. Angew Chem Int Ed Engl1985;
24:62–4
40.
WatanabeFKatsuraHAbeKNakanoY.Effect of light-induced riboflavin degradation on the loss of cobalamin in milk. J Home Econ Jpn2000;
51:231–4
BunchasakCKachanaS.Dietary folate and vitamin B12 supplementation and consequent vitamin deposition in chicken eggs. Trop Anim Health Prod2009;
41:1583–9
43.
DoscherholmenAMcMahonJRipleyD.Inhibitory effect of eggs on vitamin B12 absorption: description of a simple ovalbumin 57Co-vitamin B12 absorption test. Br J Haematol1976;
33:261–72
44.
KatsuraHInuiHDoiY.Absorption efficiency of vitamin B12 from cooked and processed foods. Its application to evaluation of vitamin B12 in the elderly. Vitamins (in Japanese)2014;
88:267–74
45.
TengFBitoTTakenakaSYabutaYWatanabeF.Yolk of the century egg (pidan) contains a readily digestible form of free vitamin B12. J Nutr Sci Vitaminol2016;
62:366–71
46.
YoshinoKInagawaMOshimaMYokotaKUmesawaMEndoMYamagashiKTanigawaTSatoSShimamotoTIsoH.Trends in dietary intake of folate, vitamin B6 and vitamin B12 among Japanese adults in two rural communities from 1971 through 2001. J Epidemiol2005;
15:29–37
47.
BourreJMEPaquottePM.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 Nutr2008;
59:491–501
48.
ScheersNLindqvistHLangkildeAMUndelandISandbergAS.Vitamin B12 as a potential compliance marker for fish intake. Eur J Nutr2014;
53:1327–33
49.
BertrandEMMcCrowJPMoustafaAZhengHMcQuaidJMDelmontTOPostAFSiplerRESpackeenJLXuKBronkDAHutchinsD.Phytoplankron-bacterial interactions mediated micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci USA2015;
112:9938–43
50.
DoxeyACKurtzDALynchMDLSauderLANeufeldJD.Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production. Isme J2015;
9:461–71
51.
HayashiMYukinoTWatanabeFMiyamotoENakanoY.Effect of vitamin B12-enriched Traustochyrids on the population growth of rotifers. Biosci Biotechnol Biochem2007;
71:222–5
52.
IshiharamYImaiETakenakaSFujitaTYabutaYWatanabeF.Characterization of a corrinoid compound from pacific bluefin tuna (Thunnus orientalis) liver. Food Sci Technol Res2011;
17:589–94
53.
AdachiSMiyamotoEWatanabeFEnomotoTKudaTHayashiMNakanoY.Purification and characterization of a corrinoid compound from Japanese salted and fermented salmon kidney ‘Mefun’. J Liq Chrom Rel Technol2005;
28:2561–9
54.
NishiokaMKanosueFYabutaYWatanabeF.Loss of vitamin B12 in fish (round herring) meats during various cooking treatments. J Nutr Sci Vitaminol2011;
57:432–6
55.
NishiokaMKanosueFTaniokaYMiyamotoEWatanabeF.Characterization of vitamin B12 in skipjack meats and loss of the vitamin from the fish meats by various cooking conditions. Vitamins (in Japanese)2006;
80:507–11
56.
WatanabeFTaniokaY. Characterization of corrinoid compounds in edible shellfish. In: Hay RM (ed) Shellfish: human consumptions, health implications and conservation concerns. New York: Nova Science Publishers, 2014, pp.413 − 20.
57.
WatanabeFKatsuraHTakenakaSEnomotoEMiyatomoENakatsukaTNakanoY.Characterization of vitamin B12 compounds from edible shellfish, clam, oyster, and mussel. Int J Food Sci Nutr2001;
52:263–8
58.
UetaKNishiokaMYabutaYWatanabeF. TLC-Banalysis of vitamin B12 compound from the short-necked clam (Ruditapes Philippinarum) extract used as a flavoring. J Liq Chrom Rel Technol2010;
33:972–9
59.
UetaKTakenakaSYabutaYWatanabeF.Broth from canned clams is suitable for use as an excellent source of free vitamin B12. J Agric Food Chem2011;
59:12054–8
60.
UetaKIshiharaYYabutaYMasudaSWatanabeF. TLC-A.of a corrinoid compound from Japanease rock-oyster “Iwa-gaki” (Crassostrea Nippona). J.Liq Chrom Rel Technol2011;
34:928–35
61.
IshiharaYUetaKBitoTTakenakaSYabutaYWatanabeF.Characterization of vitamin B12 compounds from the brackish-water bivalve Corbicula japonica. Fish Sci2013;
79:321–6
62.
TaniokaYTakenakaSFurushoTYabutaYNakanoYWatanabeF.Identification of vitamin B12 and pseudovitamin B12 from various edible shellfish using liquid chromatography-electrospray ionization/tandem mass spectrometry. Fish Sci2013;
80:1065–71
63.
DangVBenkendorffKGreenTSpeckP.Marine snails and slugs: a great place to look for antiviral drugs. J Virol2015;
89:8114–8
64.
TengFTaniokaYHamaguchiNBitoTTakenakaSYabutaYWatanabeF.Determination and chacterization of vitamin B12 compounds in edible sea snails, ivory shell Babylonia japonica and turban shell Turdo Batillus cornutus. Fish Sci2015;
81:1105–11
65.
YamadaSShibataYTakeyamaMNaritaYSugawaraKFukudaM.Content and characterization of vitamin B12 in some seaweeds. J Nutr Sci Vitaminol1996;
42:497–505
66.
TaniokaYTakenakaSFurushoTYabutaYNakanoYWatanabeF.Characterization of vitamin B12-related compounds isolated from edible portion of abalone. Vitamins (in Japanese)2012;
86:390–4
67.
TengFTaniokaYBitoTTakenakaSYabutaYWatanabeF.Occurrence of biologically inactive corrinoid compounds in canned edible apple snail (escargots). Food Nutr Sci2015;
6:1071–7
68.
AllenRHStablerSP.Identification and quantitation of cobalamin and cobalamin analogues in human feces. Am J Clin Nutr2008;
87:1324–35
69.
RothJRLawrenceJGBobikTA.Cobalamin (coenzyme B12): synthesis and biological significance. Annu Rev Microbiol1996;
50:137–81
70.
IguchiHYurimotoHSakaiY.Interactions of methylotrophs with plants and other heterotrophic bacteria. Microorganims2015;
3:137–51
71.
MinamisawaKImaizumi-AnrakuHBaoZShinodaROkuboT.Are symbiotic methanotrophs key microbes for N acquisition in paddy rice root?Microbes Environ2016;
31:4–10
72.
MiyamotoEWatanabeFYamajiRInuiHSatoKNakanoY.Purification and characterization of methylmalonyl-CoA mutase from a methanol-utilizing bacterium, methylobacterium extrorquens NR-1. J Nutr Sci Vitaminol2002;
48:242–6
73.
TaniAOguraYHayashiTKimbaraK.Complete genome sequence of methylobacterium aquaticum strain 22A, isolated from Racomitrium japonicum moss. Gen Ann2015;
3:e00266–15
74.
IguchiHYurimkotoHSakaiY.Stimulation of methanotrophic growth in cocultures by cobalamin excreted by rhizobia. Appl Environ Microbiol2011;
77:8509–15
75.
WatanabeFSchwarzJTakenakaSMiyamotoTOhishiNNelleEHochstrasserRYabutaY.Characterization of vitamin B12 compounds in the wild edible mushrooms black trumpet (Craterellus cornucopioides) and golden chanterelle (Cantharellus cibarius). J Nutr Sci Vitaminol2012;
58:50–3
76.
TengFBitoTTakenakaSYabutaYShimomuraNWatanabeF.Determination and characterization of corrinoid compounds in truffle (Tuber spp.) and shoro (Rhizopogon rubescens) fruiting bodies. Mushroom Sci Biotechnol2015;
22:159–64
77.
CroftMTLawrenceADRaux-DeeryEWarrenMJSmithAG.Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature2005;
438:90–3
78.
HelliwellKE.The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol2017;
216:62–8
79.
NakosMPepelanovaIBeutelSKringsUBergerRGScheperT.Isolation and analysis of vitamin B12 from plant samples. Food Chem2017;
216:301–8
80.
MozafarA.Enrichment of some B-vitamins in plants with application of organic fertilizers. Plant Soil1994;
167:305–11
81.
BitoTOhishiNTakenakaSYabutaYMiyamotoENishiharaEWatanabeF.Characterization of vitamin B12 compounds in biofertilizers containing purple photosynthetic bacteria. Trends Chromatogr2012;
7:23–8
82.
SatoKKudoYMuramatsuK.Incorporation of a high level of vitamin B12 into a vegetable, kaiware daikon (Japanese radish sprout), by the absorption from its seeds. Biochim Biophys Acta2004;
1672:135–7
83.
BitoTOhishiNHatanakaYTakenakaSNishiharaEYabutaYWatanabeF.Production and characterization of cyanocobalamin-enriched lettuce (Lactuca sativa L.) grown using hydroponics. J Agric Food Chem2013;
61:3852–8
84.
ShiptonMJThachilJ.Vitamin B12 deficiency-A 21st century perspective. Clin Med (Lond)2015;
15:145–50
85.
BitoTTengFOhishiNTakenakaSMiyamotoESakunoETerashimaKYabutaYWatanabeF.Characterization of vitamin B12 compounds in the fruiting bodies of shiitake mushroom (Lentinula edodes) and bed logs after fruiting of the mushroom. Mycoscience2014;
55:464–8
86.
KoyyalamudiSRJeongSCChoKYPangG.Vitamin B12 is the active corrinoid produced in cultivated white button mushrooms (Agaricus bisporus). J Agric Food Chem2009;
57:6327–33
87.
TengFBitoTTakenakaSYabutaYWatanabeF.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 Chem2014;
62:1726–32
88.
StablerSPBrassEPMarcellPDAllenRH.Inhibition of cobalamin-dependent enzymes by cobalamin analogues in rats. J Clin Invest1991;
87:1422–30
89.
BlouinNABrodieJAGrossmanACXuPBrawleySH.Porphyra: a marine crop shaped by stress. Trends Plant Sci2011;
16:29–37
90.
WatanabeFTakenakaSKittaka-KatsuraHEbaraSMiyamotoE.Characterization and bioavailability of vitamin B12 – compounds from edible algae. J Nutr Sci Vitaminol2002;
48:325–31
91.
MiyamotoEYabutaYKwakCSEnomotoTWatanabeF.Characterization of vitamin B12 compounds from Korean purple laver (Porphyra sp.) products. J Agric Food Chem2009;
57:2793–6
92.
BrawleySHBlouinNAKicko-BleanEWheelerGLohrMGoodsonHVJenkinsJWBlaby-HaasCEHelliwellKHChanCXMarriageTNBhattacharyaDKleinASBadisYBrodieJCaoYCollenJDittamiSMGachonCMMGreenBRKarpowiczSJKimJWKudahlUJLinSMichelGMittagMOlsonBJSCPangilinanJLPengYQiuHShuSSingerJSmithAGSprecherBNWagnerVWangWWangWWangZYYanJYarishCZauner-RiekSZhuangYZouYLindquistEAGrimwoodJBarryKWRokhsarDSSchmutzJStillerJWGrossmanARProchnikS.Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc Natl Acad Sci USA2017;
114:E6361−70
93.
WatanabeFYabutaYBitoTTengF.Vitamin B12-containing plant food sources for vegetarians. Nutrients2014;
6:1861–73
94.
TakenakaSSugiyamaSEbaraSMiyamotoEAbeKTamuraYWatanabeFTsuyamaSNakanoY.Feeding dried purple laver (nori) to vitamin B12-deficient rats significantly improves vitamin B12 status. Brit J Nutr2001;
85:699–703
95.
van den BergHBrandsenLSinkeldamBJ.Vitamin B12 content and bioavailability of spirulina and nori in rats. J Nutr Biochem1991;
2:314–8
96.
Kittaka-KatsuraHFujitaTWatanabeFNakanoY.Purification and characterization of a corrinoid compound from Chlorella tablets as an algal health food. J Agric Food Chem2002;
50:4994–7
97.
YangSDFengYJFuW.Determination of cobalamin in Chlorella food by cation exchange column and graphite furnace atomic absorption spectrometry. J Food Drug Anal2006;
14:50–3
98.
ChenJHJiangSJ.Determination of cobalamin in nutritive supplements and chlorella foods by capillary electrophoresis-inductively coupled plasma mass spectrometry. J Agric Food Chem2008;
56:1210–5
99.
KumudhaASelvakumarSDilshadPVaidyanathanGThakurMSSaradaR.Methylcobalamin-A form of vitamin B12 identified and characterized in Chlorella vulgaris. Food Chem2015;
170:316–20
100.
BitoTBitoMAsaiYTakenakaSYabutaYTagoKOhnishiMMizoguchiTWatanabeF.Characterization and quantitation of vitamin B12 compounds in various Chlorella supplements. J Agric Food Chem2016;
64:8516–24
101.
WatanabeFAbeKTakenakaSTamuraYMaruyamaINakanoY.Occurrence of cobalamin coenzymes in the photosynthetic green alga, Chlorella vulgaris. Biosci Biotechnol Biochem1997;
61:896–7
102.
HelliwellKHWheelerGLLeptosKCGoldsteinREMithAG.Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol Biol Evol2011;
28:2921–33
103.
DegnanPHTagaMEGoodmanAL.Vitamin B12 as a modulator of gut microbial ecology. Cell Metab2014;
20:769–78
104.
Institute of Medicine. Vitamin B12 In: Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, biotin, and choline. Washington, DC: Institute of Medicine, National Academy Press, 1998, pp.306–56
