Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 9, pp 3875–3885 | Cite as

Cobalamin is produced by Acetobacter pasteurianus DSM 3509

  • Clemens Bernhardt
  • Xuan Zhu
  • David Schütz
  • Markus Fischer
  • Bernward BispingEmail author
Applied microbial and cell physiology

Abstract

Only a few cobalamin-producing bacterial species are known which are suitable for food fermentations. The strain of Acetobacter pasteurianus DSM 3509 was found to have the capability to synthesize cobalamin. A survival test and a preliminary genetic study of the gene of uroporphyrinogen-III synthase indicated the ability to synthesize cobalamin. By a modified microbiological assay based on Lactobacillus delbrueckii ssp. lactis DSM 20355, 4.57 ng/mL of cyanocorrinoids and 0.75 ng/mL of noncorrinoid growth factors were detected. The product extracted and isolated by immunoaffinity chromatography in its cyanide form had the similar UV spectrum as standard cyanocobalamin and Coα-[α-(7-adenyl)]-(Coβ-cyano) cobamide also known as pseudovitamin B12 produced by Lactobacillus reuteri DSM 20016. The chromatographically separated product of A. pasteurianus was subjected to mass spectrometrical analysis. There, its fragmentation pattern turned out to be equivalent to that of cyanocobalamin also produced by Propionibacterium freudenreichii ssp. freudenreichii DSM 20271 and clearly differs from pseudovitamin B12. Due to the presence of this species in several food applications, there might be cobalamin residues in food fermented with these bacteria.

Keywords

Acetobacteraceae Vitamin B12 Pseudovitamin B12 Immunoaffinity chromatography 

Notes

Acknowledgments

We thank Andrew D. Farr for helpful comments and proof-reading.

Funding information

We are grateful to Deutscher Akademischer Austausch Dienst for financial support to Xuan Zhu. This work was supported by Federal Ministry of Education and Research (BMBF, Bonn-Bad Godesberg) grant 0315825.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ardhana MM, Fleet GH (2003) The microbial ecology of cocoa bean fermentations in Indonesia. Int J Food Microbiol 86:87–99.  https://doi.org/10.1016/s0168-1605(03)00081-3 CrossRefGoogle Scholar
  2. Baik HW, Russell RM (1999) Vitamin B12 deficiency in the elderly. Annu Rev Nutr 19:357–377.  https://doi.org/10.1146/annurev.nutr.19.1.357 CrossRefGoogle Scholar
  3. Blake CJ (2007) Analytical procedures for water-soluble vitamins in foods and dietary supplements: a review. Anal Bioanal Chem 389:63–76.  https://doi.org/10.1007/s00216-007-1309-9 CrossRefGoogle Scholar
  4. Camu N, De Winter T, Verbrugghe K, Cleenwerck I, Vandamme P, Takrama JS, Vancanneyt M, De Vuyst L (2007) Dynamics and biodiversity of populations of lactic acid bacteria and acetic acid bacteria involved in spontaneous heap fermentation of cocoa beans in Ghana. Appl Environ Microbiol 73:1809–1824.  https://doi.org/10.1128/AEM.02189-06 CrossRefGoogle Scholar
  5. Chamlagain B, Edelmann M, Kariluoto S, Ollilainen V, Piironen V (2015) Ultra-high performance liquid chromatographic and mass spectrometric analysis of active vitamin B12 in cells of Propionibacterium and fermented cereal matrices. Food Chem 166:630–638.  https://doi.org/10.1016/j.foodchem.2014.06.068 CrossRefGoogle Scholar
  6. Chamlagain B, Sugito TA, Deptula P, Edelmann M, Kariluoto S, Varmanen P, Piironen V (2018) In situ production of active vitamin B12 in cereal matrices using Propionibacterium freudenreichii. Food Sci Nutr 6:67–76.  https://doi.org/10.1002/fsn3.528 CrossRefGoogle Scholar
  7. Chin HB (1985) Vitamin B12. In: Augustin J, Klein BP, Becker BS, Venugopal PB (eds) Methods of vitamin assay 4edn. Wiley, New York, pp 497–514Google Scholar
  8. Crafack M, Mikkelsen MB, Saerens S, Knudsen M, Blennow A, Lowor S, Takrama J, Swiegers JH, Petersen GB, Heimdal H, Nielsen DS (2013) Influencing cocoa flavour using Pichia kluyveri and Kluyveromyces marxianus in a defined mixed starter culture for cocoa fermentation. Int J Food Microbiol 167:103–116.  https://doi.org/10.1016/j.ijfoodmicro.2013.06.024 CrossRefGoogle Scholar
  9. Crofts TS, Seth EC, Hazra AB, Taga ME (2013) Cobamide structure depends on both lower ligand availability and CobT substrate specificity. Chem Biol 20:1265–1274.  https://doi.org/10.1016/j.chembiol.2013.08.006 CrossRefGoogle Scholar
  10. Davey GK, Spencer EA, Appleby PN, Allen NE, Knox KH, Key TJ (2002) EPIC–Oxford: lifestyle characteristics and nutrient intakes in a cohort of 33 883 meat-eaters and 31 546 non meat-eaters in the UK. Public Health Nutr 6:259–268.  https://doi.org/10.1079/PHN2002430 Google Scholar
  11. De Vuyst L, Weckx S (2016) The cocoa bean fermentation process: from ecosystem analysis to starter culture development. J Appl Microbiol 121:5–17.  https://doi.org/10.1111/jam.13045 CrossRefGoogle Scholar
  12. Denter J, Bisping B (1994) Formation of B-vitamins by bacteria during the soaking process of soybeans for tempe fermentation. Int J Food Microbiol 22:23–31.  https://doi.org/10.1016/0168-1605(94)90004-3 CrossRefGoogle Scholar
  13. Deptula P, Chamlagain B, Edelmann M, Sangsuwan P, Nyman TA, Savijoki K, Piironen V, Varmanen P (2017) Food-like growth conditions support production of active vitamin B12 by Propionibacterium freudenreichii 2067 without DMBI, the lower ligand base, or cobalt supplementation. Front Microbiol 8:368.  https://doi.org/10.3389/fmicb.2017.00368 CrossRefGoogle Scholar
  14. Deptula P, Kylli P, Chamlagain B, Holm L, Kostiainen R, Piironen V, Savijoki K, Varmanen P (2015) BluB/CobT2 fusion enzyme activity reveals mechanisms responsible for production of active form of vitamin B12 by Propionibacterium freudenreichii. Microb Cell Factories 14:186.  https://doi.org/10.1186/s12934-015-0363-9 CrossRefGoogle Scholar
  15. Friedrich W (1975) Vitamin B12 und verwandte Corrinoide. Georg Thieme, StuttgartGoogle Scholar
  16. Hargrove ER, Alexandria V, Abraham L (1955) Process for the manufacture of vitamin B12 Google Scholar
  17. Hoffmann C, Stokstad E, Hutchings B, Dornbush A, Jukes TH (1949) The microbiological assay of vitamin B12 with Lactobacillus leichmannii. J Biol Chem 181:635–644Google Scholar
  18. Hugenschmidt S, Schwenninger SM, Gnehm N, Lacroix C (2010) Screening of a natural biodiversity of lactic and propionic acid bacteria for folate and vitamin B12 production in supplemented whey permeate. Int Dairy J 20:852–857.  https://doi.org/10.1016/j.idairyj.2010.05.005 CrossRefGoogle Scholar
  19. 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. Fisheries Sci 79:321–326.  https://doi.org/10.1007/s12562-013-0596-7 CrossRefGoogle Scholar
  20. Kanchanarach W, Theeragool G, Inoue T, Yakushi T, Adachi O, Matsushita K (2010) Acetic acid fermentation of Acetobacter pasteurianus: relationship between acetic acid resistance and pellicle polysaccharide formation. Biosci Biotechnol Biochem 74:1591–1597.  https://doi.org/10.1271/bbb.100183 CrossRefGoogle Scholar
  21. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731.  https://doi.org/10.1016/j.jmb.2015.11.006 CrossRefGoogle Scholar
  22. Kato K, Hayashi M, Kamikubo T (1968) Isolation of 5,6-dimethylbenzimidazolyl cobamide coenzyme as a cofactor for glutamate formation from Acetobacter suboxydans. Biochim et Biophys Acta 165:233–237CrossRefGoogle Scholar
  23. Keuth S, Bisping B (1994) Vitamin B12 production by Citrobacter freundii or Klebsiella pneumoniae during tempeh fermentation and proof of enterotoxin absence by PCR. Appl Environ Microbiol 60:1495–1499Google Scholar
  24. Kirk SFL, Cade JE, Barrett JH, Conner M (1999) Diet and lifestyle characteristics associated with dietary supplement use in women. Public Health Nutr 2:69–73.  https://doi.org/10.1017/S1368980099000099 CrossRefGoogle Scholar
  25. Lagunes Galvez S, Loiseau G, Paredes JL, Barel M, Guiraud JP (2007) Study on the microflora and biochemistry of cocoa fermentation in the Dominican Republic. Int J Food Microbiol 114:124–130.  https://doi.org/10.1016/j.ijfoodmicro.2006.10.041 CrossRefGoogle Scholar
  26. Lefeber T, Papalexandratou Z, Gobert W, Camu N, De Vuyst L (2012) On-farm implementation of a starter culture for improved cocoa bean fermentation and its influence on the flavour of chocolates produced thereof. Food Microbiol 30:379–392.  https://doi.org/10.1016/j.fm.2011.12.021 CrossRefGoogle Scholar
  27. Madhu AN, Giribhattanavar P, Narayan MS, Prapulla SG (2010) Probiotic lactic acid bacterium from kanjika as a potential source of vitamin B12: evidence from LC-MS, immunological and microbiological techniques. Biotechnol Lett 32:503–506.  https://doi.org/10.1007/s10529-009-0176-1 CrossRefGoogle Scholar
  28. Martens H, Barg M, Warren D, Jahn J-H (2002) Microbial production of vitamin B12. Appl Microbiol Biotechnol 58:275–285.  https://doi.org/10.1007/s00253-001-0902-7 CrossRefGoogle Scholar
  29. Matsutani M, Hirakawa H, Saichana N, Soemphol W, Yakushi T, Matsushita K (2012) Genome-wide phylogenetic analysis of differences in thermotolerance among closely related Acetobacter pasteurianus strains. Microbiol 158:229–239.  https://doi.org/10.1099/mic.0.052134-0 CrossRefGoogle Scholar
  30. Minervini F, Lattanzi A, De Angelis M, Di Cagno R, Gobbetti M (2012) Influence of artisan bakery- or laboratory-propagated sourdoughs on the diversity of lactic acid bacterium and yeast microbiotas. Appl Environ Microbiol 78:5328–5340.  https://doi.org/10.1128/aem.00572-12 CrossRefGoogle Scholar
  31. Moens F, Lefeber T, De Vuyst L (2014) Oxidation of metabolites highlights the microbial interactions and role of Acetobacter pasteurianus during cocoa bean fermentation. Appl Environ Microbiol 80:1848–1857.  https://doi.org/10.1128/aem.03344-13 CrossRefGoogle Scholar
  32. Nielsen DS, Teniola OD, Ban-Koffi L, Owusu M, Andersson TS, Holzapfel WH (2007) The microbiology of Ghanaian cocoa fermentations analysed using culture-dependent and culture-independent methods. Int J Food Microbiol 114:168–186.  https://doi.org/10.1016/j.ijfoodmicro.2006.09.010 CrossRefGoogle Scholar
  33. Papalexandratou Z, Falony G, Romanens E, Jimenez JC, Amores F, Daniel HM, De Vuyst L (2011) Species diversity, community dynamics, and metabolite kinetics of the microbiota associated with traditional Ecuadorian spontaneous cocoa bean fermentations. Appl Environ Microbiol 77:7698–7714.  https://doi.org/10.1128/AEM.05523-11 CrossRefGoogle Scholar
  34. Papalexandratou Z, Lefeber T, Bahrim B, Lee OS, Daniel HM, De Vuyst L (2013) Hanseniaspora opuntiae, Saccharomyces cerevisiae, Lactobacillus fermentum, and Acetobacter pasteurianus predominate during well-performed Malaysian cocoa bean box fermentations, underlining the importance of these microbial species for a successful cocoa bean fermentation process. Food Microbiol 35:73–85.  https://doi.org/10.1016/j.fm.2013.02.015 CrossRefGoogle Scholar
  35. Passos FML, Passos FJV (1985) Descrição e classificação de bactérias acéticas isoladas da fermentação do cacau, com base em uma analise numérica. Rev Microbiol 16:290–298Google Scholar
  36. Perlman D (1959) Microbial synthesis of cobamides. Adv Appl Microbiol 1:87–122.  https://doi.org/10.1016/S0065-2164(08)70476-3 CrossRefGoogle Scholar
  37. Quesada-Chanto A, Schmid-Meyer AC, Schroeder AG, Fuchter A, Carvalho-Jonas MF, Koehntopp PI, Jonas R (1998) Comparison of methods for determination of vitamin B12 in microbial material. Biotechnol Tech 12:75–77.  https://doi.org/10.1023/a:1008815812113 CrossRefGoogle Scholar
  38. Quesnel VC (1965) Agents inducing the death of cacao seeds during fermentation. J Sci Food Agric 16:441–447.  https://doi.org/10.1002/jsfa.2740160804 CrossRefGoogle Scholar
  39. Ripari V, Gänzle MG, Berardi E (2016) Evolution of sourdough microbiota in spontaneous sourdoughs started with different plant materials. Int J Food Microbiol 232:35–42.  https://doi.org/10.1016/j.ijfoodmicro.2016.05.025 CrossRefGoogle Scholar
  40. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. The J Biol Chem 278:41148–41159.  https://doi.org/10.1074/jbc.M305837200
  41. Roessner CA, Santander PJ, Scott AI (2001) Multiple biosynthetic pathways for vitamin B12: variations on a central theme. In: Vitamins & Hormones. Academic Press, pp 267–297Google Scholar
  42. Santos F, Vera JL, Lamosa P, De Valdez GF, De Vos WM, Santos H, Sesma F, Hugenholtz J (2007) Pseudovitamin B12 is the corrinoid produced by Lactobacillus reuteri CRL1098 under anaerobic conditions. FEBS Lett 581:4865–4870.  https://doi.org/10.1016/j.febslet.2007.09.012 CrossRefGoogle Scholar
  43. Scheirlinck I, Van der Meulen R, Van Schoor A, Vancanneyt M, De Vuyst L, Vandamme P, Huys G (2008) Taxonomic structure and stability of the bacterial community in Belgian sourdough ecosystems as assessed by culture and population fingerprinting. Appl Environ Microbiol 74:2414–2423.  https://doi.org/10.1128/AEM.02771-07 CrossRefGoogle Scholar
  44. Schneider Z, Stroiński A (1987) Comprehensive B12: chemistry, biochemistry, nutrition, ecology, medicine. Walter de Gruyter, Berlin, New YorkGoogle Scholar
  45. Shoolingin-Jordan PM (1998) The biosynthesis of vitamin B12: assembly of the tetrapyrrole ring system. In: Kräutler B, Arigoni D, Golding BT (eds) Vitamin B12 and B12-Proteins. WILEY-VCH, Weinheim, pp 101–118Google Scholar
  46. Sievers M, Swings J (2005) Genus 1. Acetobacter. In: Brenner DJ, Garrity GM, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology volume 2: the Proteobacteria part C the Alpha-, Beta-, Delta-, and Epsilonproteobacteria, 2nd edn. Springer, New York, pp 41–81Google Scholar
  47. Sievers M, Sellmer S, Teuber M (1992) Acetobacter europaeus sp. nov., a main component of industrial vinegar fermenters in Central Europe. Syst Appl Microbiol 15:386–392Google Scholar
  48. Silva LR, Cleenwerck I, Rivas R, Swings J, Trujillo ME, Willems A, Velázquez E (2006) Acetobacter oeni sp. nov., isolated from spoiled red wine. Int J Syst Evol Microbiol 56:21–24.  https://doi.org/10.1099/ijs.0.46000-0 CrossRefGoogle Scholar
  49. Stabler SP, Allen RH (2004) Vitamin B12 deficiency as a worldwide problem. Annu Rev Nutr 24:299–326.  https://doi.org/10.1146/annurev.nutr.24.012003.132440 CrossRefGoogle Scholar
  50. Tanioka Y, Takenaka S, Furusho T, Yabuta Y, Nakano Y, Watanabe F (2012) Characterization of vitamin B12-related compounds isolated from edible portions of abalone. Vitamins 86:390–394 (in Japanese)Google Scholar
  51. 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. Fisheries Sci 80:1065–1071.  https://doi.org/10.1007/s12562-014-0787-x CrossRefGoogle Scholar
  52. Taranto MP, Vera JL, Hugenholtz J, De Valdez GF, Sesma F (2003) Lactobacillus reuteri CRL1098 produces cobalamin. J Bacteriol 185:5643–5647.  https://doi.org/10.1128/jb.185.18.5643-5647.2003 CrossRefGoogle Scholar
  53. Vogelmann SA, Seitter M, Singer U, Brandt MJ, Hertel C (2009) Adaptability of lactic acid bacteria and yeasts to sourdoughs prepared from cereals, pseudocereals and cassava and use of competitive strains as starters. Int J Food Microbiol 130:205–212.  https://doi.org/10.1016/j.ijfoodmicro.2009.01.020 CrossRefGoogle Scholar
  54. Voigt J, Biehl B, Heinrichs H, Kamaruddin S, Marsoner GG, Hugi A (1994) In-vitro formation of cocoa-specific aroma precursors: aroma-related peptides generated from cocoa-seed protein by co-operation of an aspartic endoprotease and a carboxypeptidase. Food Chem 49:173–180.  https://doi.org/10.1016/0308-8146(94)90155-4 CrossRefGoogle Scholar
  55. Waldmann A, Koschizke JW, Leitzmann C, Hahn A (2003) Dietary intakes and lifestyle factors of a vegan population in Germany: results from the German Vegan Study. Eur J Clin Nutr 57:947–955.  https://doi.org/10.1038/sj.ejcn.1601629 CrossRefGoogle Scholar
  56. Waldmann A, Koschizke JW, Leitzmann C, Hahn A (2007) Homocysteine and cobalamin status in German vegans. Public Health Nutr 7:467–472.  https://doi.org/10.1079/PHN2003540 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Hamburg School of Food Science, Biocenter Klein Flottbek, Division of Food Microbiology and BiotechnologyUniversity of HamburgHamburgFederal Republic of Germany
  2. 2.School of Food Science and BioengineeringZhejiang Gongshang UniversityHangzhouChina
  3. 3.Hamburg School of Food Science, Division of Food ChemistryUniversity of HamburgHamburgFederal Republic of Germany

Personalised recommendations