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Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products

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Abstract

Wheat contains various essential nutrients including the B group of vitamins. However, B group vitamins, normally present in cereals-derived products, are easily removed or destroyed during milling, food processing or cooking. Lactic acid bacteria (LAB) are widely used as starter cultures for the fermentation of a large variety of foods and can improve the safety, shelf life, nutritional value, flavor and overall quality of the fermented products. In this regard, the identification and application of strains delivering health-promoting compounds is a fascinating field. Besides their key role in food fermentations, several LAB found in the gastrointestinal tract of humans and animals are commercially used as probiotics and possess generally recognized as safe status. LAB are usually auxotrophic for several vitamins although certain strains of LAB have the capability to synthesize water-soluble vitamins such as those included in the B group. In recent years, a number of biotechnological processes have been explored to perform a more economical and sustainable vitamin production than that obtained via chemical synthesis. This review article will briefly report the current knowledge on lactic acid bacteria synthesis of vitamins B2, B11 and B12 and the potential strategies to increase B-group vitamin content in cereals-based products, where vitamins-producing LAB have been leading to the elaboration of novel fermented functional foods. In addition, the use of genetic strategies to increase vitamin production or to create novel vitamin-producing strains will be also discussed.

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References

  • Bacher A, Eberhardt S, Eisenreich W, Fischer M, Herz S, Illarionov B, Kis K, Richter G (2001) Biosynthesis of riboflavin. Vitam Horm 61:1–49

    Article  CAS  Google Scholar 

  • Bailey LB, Rampersaud GC, Kauwell GP (2003) Folic acid supplements and fortification affect the risk for neural tube defects, vascular disease and cancer: evolving science. J Nutr 133:1961–1968

    Google Scholar 

  • Batifoulier F, Verny M-A, Chanliaud E, Remesy C, Demigne C (2006) Variability of B vitamin concentrations in wheat grain, milling fractions and bread products. Eur J Agron 25:163–169

    Article  CAS  Google Scholar 

  • Beck WS (2001) Cobalamin (Vitamin B12). In: Rucker RB, Suttie JW, McCormick DB, Machlin LJ (eds) Handbook of vitamins, 3rd edn. Marcel Dekker Inc, New York, pp 463–512

    Google Scholar 

  • Blanck HM, Bowman BA, Serdula MK, Khan LK, Kohn W, Woodruff BA (2002) Angular stomatitis and riboflavin status among adolescent Bhutanese refugees living in Southeastern Nepal. Am J Clin Nutr 76:430–435

    CAS  Google Scholar 

  • Bor MV, Lydeking-Olesen E, Møller J, Nexø E (2006) A daily intake of approximately 6 μg vitamin B-12 appears to saturate all the vitamin B-12-related variables in Danish postmenopausal women. Am J Clin Nutr 83:52–58

    CAS  Google Scholar 

  • Bove P, Gallone A, Russo P, Capozzi V, Albenzio M, Spano G, Fiocco D (2012) Probiotic features of Lactobacillus plantarum mutant strains. Appl Microbiol Biotechnol. 96:431–441

    Google Scholar 

  • Burgess C, O’ Connell-Motherway M, Sybesma W, Hugenholtz J, van Sinderen D (2004) Riboflavin production in Lactococcus lactis: potential for in situ production of vitamin-enriched foods? Appl Environ Microbiol 70:5769–5777

    Article  CAS  Google Scholar 

  • Burgess CM, Smid EJ, Rutten G, van Sinderen D (2006) A general method for selection of riboflavin-overproducing food grade micro-organisms. Microb Cell Factories 5:24

    Article  Google Scholar 

  • Burgess CM, Smid EJ, van Sinderen D (2009) Bacterial vitamin B2, B11 and B12 overproduction: an overview. Int J Food Micr 133:1–7

    Article  CAS  Google Scholar 

  • Capozzi V, Menga V, Digesu AM, De Vita P, van Sinderen D, Cattivelli L, Fares C, Spano G (2011) Biotechnological production of vitamin B2-enriched bread and pasta. J Agric Food Chem 59:8013–8020

    Article  CAS  Google Scholar 

  • Capozzi V, Russo P, Fragasso M, De Vita P, Fiocco D and Spano G (2012) Biotechnology and pasta-making: lactic acid bacteria as a new driver of innovation. Front Microbio 3:94

    Google Scholar 

  • Coquard D, Huecas M, Ott M, van Dijl JM, van Loon AP, Hohmann HP (1997) Molecular cloning and characterisation of the ribC gene from Bacillus subtilis: a point mutation in ribC results in riboflavin overproduction. Mol Gen Genet 254:81–84

    Article  CAS  Google Scholar 

  • Cordain L (1999) Cereal grains: humanity’s double-edged sword. In: Simopoulos AP (ed) Evolutionary aspects of nutrition and health. Diet, exercise, genetics and chronic disease. World Rev Nutr Diet vol 84. Karger, Basel, pp 19–73

    Google Scholar 

  • Crittenden RG, Martinez NR, Plaune MJ (2002) Synthesis and utilisation of folate by yoghurt starter cultures and probiotic bacteria. Int J Food Microbiol 80:217–222

    Article  CAS  Google Scholar 

  • Cuskelly GJ, Mooney KM, Young IS (2007) Folate and vitamin B12: friendly or enemy nutrients for the elderly. Proc Nutr Soc 66:548–558

    Article  CAS  Google Scholar 

  • EFSA (2007) Opinion of the scientific committee on a request from EFSA on the introduction of a qualified presumption of safety (QPS) approach for assessment of selected microorganisms referred to EFSA. EFSA J 587:1–16

    Google Scholar 

  • European Food Information Council. MINI GUIDE 06/2006, http://www.eufic.org/article/en/expid/miniguide-vitamins/#3.

  • Finglas PM, Wright AJ, Wolfe CA, Hart DJ, Wright DM, Dainty JR (2003) Is there more to folates than neural-tube defects? Proc Nutr Soc 62:591–598

    Article  CAS  Google Scholar 

  • Flynn A, Moreiras O, Stehle P, Fletcher RJ, Muller DJ, Rolland V (2003) Vitamins and minerals: a model for safe addition to foods. Eur J Nutr 42:118–130

    Article  CAS  Google Scholar 

  • Food and Drug Administration (1996) Food standards: amendment of standards of identity for enriched grain products to require addition of folic acid. Fed Regist 61:8781–8807

    Google Scholar 

  • Gobbetti M, Corsetti A (1997) Lactobacillus sanfrancisco a key sourdough lactic acid bacterium: a review. Food Microbiol 14:175–187

    Article  CAS  Google Scholar 

  • Gobbetti M, De Angelis M, Corsetti A, Di Cagno R (2005) Biochemistry and physiology of sourdough lactic acid bacteria. Trends Food Sci Technol 16:57–69

    Article  CAS  Google Scholar 

  • Herranen M, Kariluoto S, Edelmann M, Piironen V, Ahvenniemi K, Iivonen V, Salovaara H, Korhola M (2010) Isolation and characterization of folate-producing bacteria from oat bran and rye flakes. Int J Food Microbiol 142:277–285

    Article  CAS  Google Scholar 

  • Hugenholtz J, Smid EJ (2002) Nutraceutical production with food-grade microorganisms. Curr Opin Biotechnol 13:497–507

    Article  CAS  Google Scholar 

  • Jägerstad M, Piironen V, Walker C, Ros G, Carnovale E, Holasova M, Nau H (2005) Increasing natural food folates through bioprocessing and biotechnology. Trends Food Sci Tech 16:298–306

    Article  Google Scholar 

  • Kariluoto S, Vahteristo L, Salovaara H, Katina K, Liukkonen K-H, Piironen V (2004) Effect of baking method and fermentation on folate content of rye and wheat breads. Cereal Chem 81:134–139

    Article  CAS  Google Scholar 

  • Kariluoto S, Aittamaa M, Korhola M, Salovaara H, Vahteristo L, Piironen V (2006) Effects of yeasts and bacteria on the levels of folates in rye sourdoughs. Int J Food Microbiol 106:137–143

    Article  CAS  Google Scholar 

  • Kariluoto S, Edelmann M, Piironen V (2010) Effect of environment on folate contents in wheat genotypes. J Agric Food Chem 58:9324–9331

    Article  CAS  Google Scholar 

  • Katan MB, Boekschoten MV, Connor WE, Mensink RP, Seidell J, Vessby B, Willett W (2009) Which are the greatest recent discoveries and the greatest future challenges in nutrition? Eur J Clin Nutr 63:2–10

    Article  CAS  Google Scholar 

  • Kil YV, Mironov VN, Gorishin I, Kreneva RA, Perumov DA (1992) Riboflavin operon of Bacillus subtilis: unusual symmetric arrangement of the regulatory region. Mol Gen Genet 233:483–486

    Article  CAS  Google Scholar 

  • Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100:1990–1995

    Article  CAS  Google Scholar 

  • Kumar S, Ghosh K, Das KC (1989) Serum B12 levels in an Indian population: an evaluation of three assay methods. Med Lab Sci 46:120–126

    CAS  Google Scholar 

  • Laiño JE, LeBlanc JG, Savoy de Giori G (2012) Production of natural folates by lactic acid bacteria starter cultures isolated from artisanal Argentinean yogurts Canadian. J Microbiol 58:581–588

    Google Scholar 

  • LeBlanc JG, Burgess C, Sesma F, Savoy de Giori G, van Sinderen D (2005) Ingestion of milk fermented by genetically modified Lactococcus lactis improves the riboflavin status of deficient rats. J Dairy Sci 88:3435–3442

    Article  CAS  Google Scholar 

  • LeBlanc JG, Rutten G, Bruinenberg P, Sesma F, de Giori GS, Smid EJ (2006) A novel dairy product fermented with Propionibacterium freudenreichii improves the riboflavin status of deficient rats. Nutrition 22:645–651

    Article  CAS  Google Scholar 

  • LeBlanc JG, Savoy de Giori G, Smid EJ, Hugenholtz J, Sesma F (2007) Folate production by lactic acid bacteria and other food-grade microorganisms. In: Méndez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology. Formatex Research Center, Badajoz, pp 329–339

    Google Scholar 

  • LeBlanc JG, Taranto MP, Molina V, Sesma F (2010a) B-group vitamins production by probiotic lactic acid bacteria. In: Mozzi F, Raya R, Vignolo G (eds) Biotechnology of lactic acid bacteria: novel applications. Wiley-Blackwell, Ames, pp 211–232

    Chapter  Google Scholar 

  • LeBlanc JG, Sybesma W, Starrenburg M, Sesma F, de Vos WM, de Giori GS, Hugenholtz J (2010b) Supplementation with engineered Lactococcus lactis improves the folate status in deficient rats. Nutrition 26:835–841

    Article  CAS  Google Scholar 

  • LeBlanc JG, van Sinderen D, Hugenholtz J, Piard J-C, Sesma F, Savoy de Giori G (2010c) Risk assessment of genetically modified lactic acid bacteria using the concept of substantial equivalence. Curr Microbiol 61:590–595

    Article  CAS  Google Scholar 

  • LeBlanc JG, Laiño JE, del Valle MJ, Vannini V, van Sinderen D, Taranto MP, de Valdez GF, de Giori GS, Sesma F (2011) B-group vitamin production by lactic acid bacteria—current knowledge and potential applications. J Appl Microbiol 111:1297–1309

    Article  CAS  Google Scholar 

  • Leklem JE (2001) Vitamin B6. In: Rucker RB, Suttie JW, McCormick DB, Machlin LJ (eds) Handbook of vitamins, 3rd edn. Marcel Dekker Inc, New York, pp 339–396

    Google Scholar 

  • Lin MY, Young CM (2000) Folate levels in cultures of lactic acid bacteria. Int Dairy J 10:409–413

    Article  CAS  Google Scholar 

  • Massey V (2000) The chemical and biological versatility of riboflavin. Biochem Soc Trans 28:283–296

    Article  CAS  Google Scholar 

  • Morita H, Toh H, Fukuda S, Horikawa H, Oshima K, Suzuki T, Murakami M, Hisamatsu S, Kato Y, Takizawa T, Fukuoka H, Yoshimura T, Itoh K, O’Sullivan DJ, McKay LL, Ohno H, Kikuchi J, Masaoka T, Hattori M (2008) Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res 15:151–161

    Article  CAS  Google Scholar 

  • Nor NM, Mohamad R, Foo HL, Rahim RA (2010) Improvement of folate biosynthesis by lactic acid bacteria using response surface methodology. Food Tech Biotechnol 48:243–250

    CAS  Google Scholar 

  • Food and Nutrition Board (1998) Folate. In: Dietary reference intakes: thiamin, riboflavin, niacin, vitamin B6, vitamin B12, pantothenic acid, biotin, folate and choline. National Academies Press, Washington, pp 196–305

  • O’Brien MM, Kiely M, Harrington KE, Robson PJ, Strain JJ, Flynn A (2001) The North/South Ireland food consumption survey: vitamin intakes in 18–64-year-old adults. Publ Health Nutr 4:1069–1079

    Google Scholar 

  • Osseyi ES, Wehling RL, Albrecht JA (2001) HPLC determination of stability and distribution of added folic acid and some endogenous folates during breadmaking. Cereal Chem 78:375–378

    Article  CAS  Google Scholar 

  • Perkins J, Sloma A, Hermann T, Theriault K, Zachgo E, Erdenberger T, Hannett N, Chatterjee N, Williams V II, Rufo GA Jr, Hatch R, Pero J (1999) Genetic engineering of Bacillus subtilis for the commercial production of riboflavin. J Ind Microbiol Biotechnol 22:8–18

    Article  CAS  Google Scholar 

  • Piao Y, Yamashita M, Kawaraichi N, Asegawa R, Ono H, Murooka Y (2004) Production of vitamin B12 in genetically engineered Propionibacterium freudenreichii. J Biosci Bioeng 98:167–173

    CAS  Google Scholar 

  • Powers HJ (2003) Riboflavin (vitamin B2) and health. Am J Clin Nutr 77:1352–1360

    CAS  Google Scholar 

  • Rao DR, Reddy AV, Pulusani SR, Cornwell PE (1984) Biosynthesis and utilization of folic acid and vitamin B12 by lactic acid cultures in skim milk. J Dairy Sci 67:1169–1174

    Article  CAS  Google Scholar 

  • Rivlin RS, Pinto JT (2001) Riboflavin (vitamin B2). In: Rucker RB, Suttie JW, McCormick DB, Machlin LJ (eds) Handbook of vitamins, 3rd edn. Marcel Dekker Inc, New York, pp 255–275

    Google Scholar 

  • Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278:41148–41159

    Article  CAS  Google Scholar 

  • Rohner F, Zimmermann MB, Wegmueller R, Tschannen AB, Hurrell RF (2007) Mild riboflavin deficiency is highly prevalent in school-age children but does not increase risk for anaemia in Côte d’Ivoire. Br J Nutr 97:970–976

    Article  CAS  Google Scholar 

  • Rossi M, Amaretti A, Raimondi S (2011) Folate production by probiotic bacteria. Nutrients 3:118–134

    Article  CAS  Google Scholar 

  • Russo P, López P, Capozzi V, Palencia P, Dueñas MT, Spano G, Fiocco D (2012) Beta-glucans improve growth, viability and colonization of probiotic microorganisms. Int J Mol Sci 13:6026–6039

    Article  CAS  Google Scholar 

  • Santos F, Vera JL, Lamosa P, de Valdez GF, de Vos W, 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

    Article  CAS  Google Scholar 

  • Santos F, Wegkamp A, de Vos WM, Smid EJ, Hugenholtz J (2008a) High folate production in fermented foods by the B12 producer Lactobacillus reuteri JCM1112. Appl Environ Microbiol 74:3291–3294

    Article  CAS  Google Scholar 

  • Santos F, Vera JL, van der Heijden R, Valdez G, de Vos WM, Sesma F, Hugenholtz J (2008b) The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. Microbiology 154:81–93

    Article  CAS  Google Scholar 

  • Scott JM (1999) Folate and vitamin B12. Proc Nutr Soc 58:441–448

    Article  CAS  Google Scholar 

  • Seidametova EA, Shakirzianova MR, Ruzieva DM, Guliamova TG (2004) Isolation of cobalt-resistant strains of propionic acid bacteria, potent producers of vitamin B12. Appl Biochem Microbiol 40:560–562

    Article  CAS  Google Scholar 

  • Selhub J (2002) Folate, vitamin B12 and vitamin B6 and one carbon metabolism. J Nutr Health Aging 6:39–42

    CAS  Google Scholar 

  • Sriramulu DD, Liang M, Hernandez-Romero D, Raux-Deery E, Lünsdorf H, Parsons JB, Warren MJ, Prentice MB (2008) Lactobacillus reuteri DSM 20016 produces cobalamin-dependent diol dehydratase in metabolosomes and metabolizes 1,2-propanediol by disproportionation. J Bacteriol 190:4559–4567

    Article  CAS  Google Scholar 

  • Stanton C, Ross RP, Fitzgerald GF, Sinderen DV (2005) Fermented functional foods based on probiotics and their biogenic metabolites. Curr Opin Biotechnol 16:198–203

    Article  CAS  Google Scholar 

  • Sybesma W, Starrenburg M, Tijsseling L, Hoefnagel MH, Hugenholtz J (2003a) Effects of cultivation conditions on folate production by lactic acid bacteria. Appl Environ Microbiol 69:4542–4548

    Article  CAS  Google Scholar 

  • Sybesma W, Starrenburg M, Kleerebezem M, Mierau I, de Vos WM, Hugenholtz J (2003b) Increased production of folate by metabolic engineering of Lactococcus lactis. Appl Environ Microbiol 69:3069–3076

    Article  CAS  Google Scholar 

  • Sybesma W, Burgess C, Starrenburg M, van Sinderen D, Hugenholtz J (2004) Multivitamin production in Lactococcus lactis using metabolic engineering. Metab Eng 6:109–115

    Article  CAS  Google Scholar 

  • Taboada B, Verde C, Merino E (2010) High accuracy operon prediction method based on STRING database scores. Nucleic Acids Res 38:e130

    Article  Google Scholar 

  • Tanphaichitr V (2001) Thiamine. In: Rucker RB, Suttie JW, McCormick DB, Machlin LJ (eds) Handbook of vitamins, 3rd edn. Marcel Dekker Inc., New York, pp 275–310

    Google Scholar 

  • Taranto MP, Vera JL, Hugenholtz J, De Valdez GF, Sesma F (2003) Lactobacillus reuteri CRL1098 produces cobalamin. J Bacteriol 185:5643–5647

    Article  CAS  Google Scholar 

  • Tucker KL, Olson B, Bakun P, Dallal GE, Selhub J, Rosenberg IH (2004) Breakfast cereal fortified with folic acid, vitamin B-6, and vitamin B-12 increases vitamin concentrations and reduces homocysteine concentrations: a randomized trial. Am J Clin Nutr 79:805–811

    CAS  Google Scholar 

  • Vogel RF, Pavlovic M, Ehrmann MA, Wiezer A, Liesegang H, Offschanka S, Voget S, Angelov A, Böcker G, Liebl W (2011) Genomic analysis reveals Lactobacillus sanfranciscensis as stable element in traditional sourdoughs. Microb Cell Factories 10:S6

    Article  Google Scholar 

  • Watanabe F (2007) Vitamin B12 sources and bioavailability. Exp Biol Med 232:1266–1274

    Article  CAS  Google Scholar 

  • Wegkamp A (2008) Modulation of folate production in lactic acid bacteria. PhD thesis. Wageningen, The Netherlands: Wageningen University

  • Wegkamp A, van Oorschot W, de Vos WM, Smid EJ (2007) Characterization of the role of para- aminobenzoic acid biosynthesis in folate production by Lactococcus lactis. Appl Environ Microbiol 73:2673–2681

    Article  CAS  Google Scholar 

  • Wels M, Francke C, Kerkhoven R, Kleerebezem M, Siezen RJ (2006) Predicting cis acting elements of Lactobacillus plantarum by comparative genomics with different taxonomic subgroups. Nucleic Acids Res 34:1947–1958

    Article  CAS  Google Scholar 

  • Zhu T, Pan Z, Domagalski N, Koepsel R, Ataai MM, Domach MM (2005) Engineering of Bacillus subtilis for enhanced total synthesis of folic acid. Appl Environ Microbiol 71:7122–7129

    Article  CAS  Google Scholar 

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Acknowledgements

This work was founded by the Italian Ministry for Development in the framework of the “Industria 2015 Bando Nuove Tecnologie per il Made in Italy—Realizzazione di una innovativa pasta alimentare funzionale arricchita di componenti bioattivi e probiotici.” This paper is dedicated to the memory of our friend and colleague, Dr. Natale di Fonzo.

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Authors and Affiliations

  1. Department of Agriculture, Food and Environment Sciences, University of Foggia, via Napoli 25, 71122, Foggia, Italy

    Vittorio Capozzi, Pasquale Russo & Giuseppe Spano

  2. Department of Applied Chemistry, University of Basque Country (UPV/EHU), Paseo Manuel de Lardizábal 3, 20018, Donostia, Spain

    María Teresa Dueñas

  3. Department of Molecular Microbiology and Infection Biology, Centro de Investigaciones Biológicas (CIB), Madrid, Spain

    Paloma López

  4. Promis Biotech srl, via Napoli 25, 71122, Foggia, Italy

    Vittorio Capozzi & Pasquale Russo

  5. Department of Agriculture, Food and Environment Sciences, University of Foggia, via Napoli, 25, 71122, Foggia, Italy

    Giuseppe Spano

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  1. Vittorio Capozzi
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Capozzi, V., Russo, P., Dueñas, M.T. et al. Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products. Appl Microbiol Biotechnol 96, 1383–1394 (2012). https://doi.org/10.1007/s00253-012-4440-2

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