Lactic acid bacteria as a cell factory for riboflavin production

Microbial Biotechnology

Volumn 9, Issue 4, 2016, Pages 441-451

  Thakur, Kiran ^a   Tomar, Sudhir Kumar ^a   De, Sachinandan ^a  

^a NATIONAL DAIRY RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOFLAVIN;

BACTERIAL GENE; BACTERIAL STRAIN; BIOSYNTHESIS; COMMENSAL; ENTEROCOCCUS FAECALIS; FOOD INDUSTRY; FOOD PROCESSING; FORTIFICATION; GENETIC ENGINEERING; HUMAN; LACTIC ACID BACTERIUM; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS AMYLOVORUS; LACTOBACILLUS BREVIS; LACTOBACILLUS BUCHNERI; LACTOBACILLUS CASEI; LACTOBACILLUS CRISPATUS; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; LACTOBACILLUS FERMENTUM; LACTOBACILLUS GASSERI; LACTOBACILLUS HELVETICUS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS KEFIRANOFACIENS; LACTOBACILLUS PLANTARUM; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SALIVARIUS; LACTOCOCCUS LACTIS; LEUCONOSTOC MESENTEROIDES; LISTERIA MONOCYTOGENES; NONHUMAN; PROMOTER REGION; REVIEW; RIBA GENE; RIBE GENE; RIBG GENE; RIBH GENE; RIBP1 GENE; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES; VITAMIN INTAKE;

EID: 84976588026     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12335     Document Type: Review

References (83)

1. Arena, M.P., Russo, P., Capozzi, V., Lopez, P., Fiocco, D., and Spano, G. (2014a) Probiotic abilities of riboflavin-overproducing Lactobacillus strains: a novel promising application of probiotics. Appl Microbiol Biotechnol 98: 7569–7581.
2. Arena, M.P., Caggianiello, G., Fiocco, D., Russo, P., Torelli, M., Spano, G., and Capozzi, V. (2014b) Barley β-glucans-containing food enhances probiotic performances of beneficial bacteria. Int J Mol Sci 15: 3025–3039.
3. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., et al. (2011) Enterotypes of the human gut microbiome. Nature 473: 174–180.
4. Ashoori, M., and Saedisomeolia, A. (2014) Riboflavin (vitamin B2) and oxidative stress: a review. Br J Nutr 20: 1–7.
5. Bacher, A., Eberhardt, S., and Richter, G. (1996) Biosynthesis of riboflavin. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC, USA: ASM Press, pp. 657–664.
6. Blanck, H.M., Bowman, B.A., Serdula, M.K., Khan, L.K., Kohn, W., and Woodruff, B.A. (2002) Angular stomatitis and riboflavin status among adolescent Bhutanese refugees living in southeastern Nepal. Am J Clin Nutr 76: 430–435.
7. Bodiga, V.L., Bodiga, S., Surampudi, S., Boindala, S., Putcha, U., Nagalla, B., et al. (2012) Effect of vitamin supplementation on cisplatin-induced intestinal epithelial cell apoptosis in Wistar/NIN rats. Nutrition 28: 572–580.
8. Burgess, C., O'Connell-Motherway, M., Sybesma, W., Hugenholtz, J., and van Sinderen, D. (2004) Riboflavin production in Lactococcus lactis: potential for in situ production of vitamin-enriched foods. Appl Environ Microbiol 70: 5769–5777.
9. Burgess, C.M., Smid, E.J., Rutten, G., and van Sinderen, D. (2006) A general method for selection of riboflavin-overproducing food grade micro-organisms. Microb Cell Fact 5: 24. doi:10.1186/1475-2859-5-24.
10. 12 overproduction: an overview. Int J Food Microbiol 133: 1–7.
11. 2-enriched bread and pasta. J Agr Food Chem 59: 8013–8020.
12. Capozzi, V., Russo, P., Duenas, M.T., Lopez, P., and Spano, G. (2012) Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products. Appl Microbiol Biotechnol 96: 1383–1394.
13. Combs, G.F. (1992) The Vitamins: Fundamental Aspects in Nutrition and Health. San Diego, CA, USA: Academic Press.
14. Cooperman, J.M., and Lopez, R. (1991) Riboflavin. In Handbook of Vitamins. Machlin, L.J. (ed.). New York, NY, USA: Marcel Dekker.
15. Coquard, D.1., Huecas, M., Ott, M., van Dijl, J.M., van Loon, A.P., and Hohmann, H.P. (1997) Molecular cloning and characterisation of the ribC gene from Bacillus subtilis: a point mutation in ribC results in riboflavin overproduction. Mol Gen Genet 54: 81–84.
16. Corbett, A.J., Eckle, S.B., Birkinshaw, R.W., Liu, L., Patel, O., Mahony, J., et al. (2014) T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509: 361–365.
17. Fischer, M., and Bacher, A. (2005) Biosynthesis of flavocoenzymes. Nat Prod Rep 22: 324–350.
18. Flynn, A., Moreiras, O., Stehle, P., Fletcher, R.J., Muller, D.J., and Rolland, V. (2003) Vitamins and minerals: a model for safe addition to foods. Eur J Nutr 42: 118–130.
19. Foley, A.R., Menezes, M.P., Pandraud, A., Gonzalez, M.A., Al-Odaib, A., Abrams, A.J., et al. (2014) Treatable childhood neuronopathy caused by mutations in riboflavin transporter RFVT2. Brain 137: 44–56.
20. 12, Pantothenic Acid, Biotin, Folate and Choline. Washington DC, USA: National Academies Press, pp. 87–122.
21. Gelfand, M.S., Mironov, A.A., Jomantas, J., Kozlov, Y.I., and Perumov, D.A. (1999) A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet 15: 439–442.
22. Guru, V., and Viswanathan, K. (2013) Riboflavin production in milk whey using probiotic bacteria – Lactobacillus acidophilus and Lactococcus lactis. Ind J Fund Appl Life Sci 3: 169–176.
23. Hassan, I., Chibber, S., and Naseem, I. (2013) Vitamin B2: a promising adjuvant in cisplatin based chemoradiotherapy by cellular redox management. Food Chem Toxicol 59: 715–723.
24. Hill, D.I., and Nalubola, R. (2002) Fortification strategies to meet micronutrient needs: successes and failures. Proc Nutr Soc 61: 231–241.
25. Hill, M.J. (1997) Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6: S43–S45.
26. Hugenholtz, J., Sybesma, W., Groot, M.N., Wisselink, W., Ladero, V., Burgess, K., et al. (2002) Metabolic engineering of lactic acid bacteria for the production of nutraceuticals. Antonie Van Leeuwenhoek 82: 217–235.
27. Ichihashi, T., Takagishi, Y., Uchida, K., and Yamada, H. (1992) Colonic absorption of menaquinone-4 and menaquinone-9 in rats. J Nutr 122: 506–512.
28. Jayashree, S., Jayaraman, K., and Kalaichelvan, G. (2010) Isolation, screening and characterization of riboflavin producing lactic acid bacteria from Katpadi, Vellore district. Recent Res Sci Technol 2: 83–88.
29. Jayashree, S., Rajendhran, J., Jayaraman, K., Kalaichelvana, G., and Gunasekaran, P. (2011) Improvement of riboflavin production by Lactobacillus fermentum isolated from yogurt. Food Biotechnol 25: 240–251.
30. Kleerebezem, M., Boekhorst, J., van Kranenburg, R., Molenaar, D., Kuipers, O.P., Leer, R., et al. (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci 100: 1990–1995.
31. Koser, S.A. (1968) Vitamin Requirements of Bacteria and Yeasts. Springfield, IL, USA: Charles C. Thomas.
32. Laino, J.E., Juarez del Valle, M., Savoy de Giori, G., and LeBlanc, J.G.J. (2012) Development of a high folate concentration yogurt naturally bio-enriched using selected lactic acid bacteria. LWT Food Sci Technol 54: 1–5.
33. LeBlanc, J.G., Burgess, C., Sesma, F., Savoy de Giori, G., and van Sinderen, D. (2005a) Ingestion of milk fermented by genetically modified Lactococcus lactis improves the riboflavin status of deficient rats. J Dairy Sci 88: 3435–3442.
34. LeBlanc, J.G., Burgess, C., Sesma, F., de Giori, G.S., and van Sinderen, D. (2005b) Lactococcus lactis is capable of improving the riboflavin status in deficient rats. Br J Nutr 94: 262–267.
35. LeBlanc, J.G., Rutten, G., Bruinenberg, P., Sesma, F., de Giori, G.S., and Smid, E.J. (2006) A novel product fermented with Propionibacterium freudenreichii improves the riboflavin status of deficient rats. Nutrition 22: 645–651.
36. LeBlanc, J.G., Laino, J.E., del Vall, M.J., Vannini, V., van Sinderen, D., Taranto, M.P., et al. (2011) B-group vitamin production by lactic acid bacteria – current knowledge and potential applications. J Appl Microbiol 111: 1297–1309.
37. LeBlanc, J.G., Milani, C., de Giori, G.S., Sesma, F., van Sinderen, D., and Ventura, M. (2012) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opinion Biotechnol 24: 160–168.
38. Magnusdottir, S., Ravcheev, D., de Crecy-Lagard, V., and Thiele, I. (2015) Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 6: 148. doi:10.3389/fgene.2015.00148.
39. Mal, P., Dutta, K., Bandyopadhyay, D., Basu, A., Khan, R., and Bishayi, B. (2013) Azithromycin in combination with riboflavin decreases the severity of Staphylococcus aureus infection induced septic arthritis by modulating the production of free radicals and endogenous cytokines. Inflammat Res 62: 259–273.
40. Marques, T.M., Wall, R., Ross, R.P., Fitzgerald, G.F., Ryan, C.A., and Stanton, C. (2010) Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opinion Biotechnol 21: 149–156.
41. Massey, V. (2000) The chemical and biological versatility of riboflavin. Biochem Soc T 28: 283–296.
42. Mensink, G.B., Fletcher, R., Gurinovic, M., Huybrechts, I., Lafay, L., Serra-Majem, L., et al. (2013) Mapping low intake of micronutrients across Europe. Br J Nutr 110: 755–773.
43. Milani, C., Lugli, G.A., Duranti, S., Turroni, F., Bottacini, F., Mangifesta, M., et al. (2014) Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl Environ Microbiol 80: 6290–6302.
44. Moat, S.J., Ashfield-Watt, P.A., Powers, H.J., Newcombe, R.G., and McDowell, I.F. (2003) Effect of riboflavin status on the homocysteine-lowering effect of folate in relation to the MTHFR (C677T) genotype. Clin Chem 49: 295–302.
45. O'Brien, M.M., Kiely, M., Harrington, K.E., Robson, P.J., Strain, J.J., and Flynn, A. (2001) The North/South Ireland Food Consumption Survey: vitamin intakes in 18–64-year-old adults. Public Health Nutr 4: 1069–1079.
46. Perkins, J., and Pero, J. (2002) Biosynthesis of riboflavin, biotin, folic acid, and cobalamin. In Bacillus subtilis and Its Closest Relatives: From Genes to Cells. Sonenshine, A., Hoch, J., and Losick, R. (eds). Washington, DC, USA: ASM Press, pp. 271–276.
47. Perkins, J.B., Pero, J.G., and Sloma, A. (1991) Riboflavin overproducing strains of bacteria. European patent application 0405370.
48. Perkins, J.B., Sloma, A., Hermann, T., Theriault, K., Zachgo, E., Erdenberger, T., et al. (1999) Genetic engineering of Bacillus subtilis for the commercial production of riboflavin. J Ind Microbiol Biot 22: 8–18.
49. Pophaly, S.D., Poonam, Singh, P., Kumar, H., Tomar, S.K., and Singh, R. (2014) Selenium enrichment of lactic acid bacteria and bifidobacteria: a functional food perspective. Trends food sci tech 39: 135–145.
50. Powers, H.J. (2003) Riboflavin (vitamin B2) and health. Am J Clin Nutr 77: 1352–1360.
51. Powers, H.J., Weaver, L.T., Austin, S., and Beresford, J.K. (1993) A proposed intestinal mechanism for the effect of riboflavin deficiency on iron loss in the rat. Brit J Nutr 69: 553–561.
52. Richter, G., Volk, R., Krieger, C., Lahm, H.W., Rothlisberger, U., and Bacher, A. (1992) Biosynthesis of riboflavin: cloning, sequencing, and expression of the gene coding for 3,4-dihydroxy-2-butanone 4-phosphate of Escherichia coli. J Bacteriol 174: 4050–4056.
53. Richter, G., Ritz, H., Katzenmeier, G., Volk, R., Kohnle, A., Lottspeich, F., et al. (1993) Biosynthesis of riboflavin: cloning, sequencing, and mapping, and expression of the gene coding for GTP cyclohydrolase II of Escherichia coli. J Bacteriol 175: 4045–4051.
54. Richter, G., Fischer, M., Krieger, C., Eberhardt, S., Lüttgen, H., Gerstenschläger, I., and Bacher, A. (1997) Biosynthesis of riboflavin: characterization of the bifunctional deaminase-reductase of Escherichia coli and Bacillus subtilis. J Bacteriol 179: 2022–2028.
55. Rohner, F., Zimmermann, M.B., Wegmueller, R., Tschannen, A.B., and Hurrell, R.F. (2007) Mild riboflavin deficiency is highly prevalent in school-age children but does not increase risk for anaemia in Cote d'Ivoire. Brit J Nutr 97: 970–976.
56. Russo, P., Lopez, P., Capozzi, V., de Palencia, P.F., Duenas, M.T., Spano, G., and Fiocco, D. (2012) Beta-glucans improve growth, viability and colonization of probiotic microorganisms. Int J Mol Sci 13: 6026–6039.
57. Russo, P., Capozzi, V., Arena, M.P., Spadaccino, G., Duenas, M.T., Lopez, P., et al. (2014) Riboflavin-overproducing strains of Lactobacillus fermentum for riboflavin-enriched bread. Appl Microbiol Biotechnol 98: 3691–3700.
58. Russo, P., Iturria, I., Mohedano, M.L., Caggianiello, G., Rainieri, S., Fiocco, D., et al. (2015) Zebrafish gut colonization by mCherry-labelled lactic acid bacteria. Appl Microbiol Biotechnol 99: 3479–3490.
59. Said, H.M., and Mohammed, Z.M. (2006) Intestinal absorption of water soluble vitamins: an update. Curr Opin Gastroenterol 22: 140–146.
60. Saini, K., Tomar, S.K., Sangwan, V., and Bhushan, B. (2014) Evaluation of Lactobacilli from human sources for uptake and accumulation of selenium. Biol Trace Elem Res 160: 433–436.
61. 2 secretion by bacteria growing on solid media. J App Microbiol 95: 1255–1260.
62. Schallmey, M., Singh, A., and Ward, O.P. (2004) Developments in the use of Bacillus species for industrial production. Can J Microbiol 50: 1–17.
63. Schetzek, S., Heinen, F., Kruse, S., Borggraefe, I., Bonfert, M., Gaul, C., et al. (2013) Headache in children: update on complementary treatments. Neuropediatrics 44: 25–33.
64. Sherwood, M.D., Ran, D., and Goldman, M.D. (2014) Effectiveness of riboflavin in pediatric migraine prevention. Can Fam Physician mars 60: 157–159.
65. Shi, S., Shen, Z., Chen, X., Chen, T., and Zhao, X. (2009) Increased production of riboflavin by metabolic engineering of the purine pathway in Bacillus subtilis. Biochem Eng J 46: 28–33.
66. Shi, Z., Zhen, S., Wittert, G.A., Yuan, B., Zuo, H., and Taylor, A.W. (2014) Inadequate riboflavin intake and anemia risk in a Chinese population: five-year follow up of the Jiangsu Nutrition Study. PLoS ONE 9: e88862.
67. Snell, E.E., and Strong, F.M. (1939) A microbiological assay for riboflavin. Ind Eng Chem, Anal ed 11: 346–350.
68. Stahmann, K.P., Revuelta, J.L., and Seulberger, H. (2000) Three biotechnical processes using Ashbya gossypii, Candida famata, or Bacillus subtilis compete with chemical riboflavin production. Appl Microbiol Biotechnol 53: 509–516.
69. Stanton, C., Ross, R.P., Fitzgerald, G.F., and Van Sinderen, D. (2005) Fermented functional foods based on probiotics and their biogenic metabolites. Curr Opinion Biotechnol 16: 198–203.
70. Sybesma, W., Burgess, C., Starrenburg, M., van Sinderen, D., and Hugenholtz, J. (2004) Multivitamin production in Lactococcus lactis using metabolic engineering. Metab Eng 6: 109–115.
71. Sybesma, W., Hugenholtz, J., de Vos, W., and Smid, E.J. (2006) Safe use of genetically modified lactic acid bacteria in food: bridging the gap between consumers, green groups, and industry. Elect J Biotechnol 9: 424–448.
72. Tamime, D.A., Tamime, A.Y., Saarela, M., Sondergaard, A.K., Mistry, V.V., and Shah, N.P. (2005) Production and maintenance of viability of probiotic micro-organisms in dairy products. In Probiotic Dairy Products.UK. Tamine, A.Y. (ed.). Oxford, UK: Blackwell Publishing, pp. 39–72.
73. Thakur, K., and Tomar, S.K. (2015) Exploring indigenous Lactobacillus species from diverse niches for riboflavin production. J Young Pharmacists 7: 122–127.
74. Thakur, K., Gosh, S., Kadam, J., and Tomar, S.K. (2015) Adhesion properties of riboflavin producing Lactobacillus mucosae isolated from human faeces. J Cell Tissue Res 15: 5095–5100.
75. Vaesken, S.M., Aperte, A.E., and Moreiras, V.G. (2012) Vitamin food fortification today. Food Nutr Res 56: 5459. doi:10.3402/fnr.v56i0.5459.
76. Valle, J.D.M., Lainoa, J.E.G., Savoy, D.G.G., and LeBlanc, J.G. (2014) Riboflavin producing lactic acid bacteria as a biotechnological strategy to obtain bio-enriched soymilk. Food Res Int 62: 1015–1019.
77. Van Loon, A.P.G.M., Hohmann, H.P., and Bretzel, W.M. (1996) Development of a fermentation process for the manufacture of riboflavin. Chimia (Aarau) 50: 410–412.
78. Ventura, M., Canchaya, C., Fitzgerald, G.F., Gupta, R.S., and van Sinderen, D. (2007) Genomics as a means to understand bacterial phylogeny and ecological adaptation: the case of bifidobacteria. Antonie Van Leeuwenhoek 91: 351–372.
79. Vitreschak, A.G., Rodionov, D.A., Mironov, A.A., and Gelfand, M.S. (2002) Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res 30: 3141–3151.
80. Wacker, J., Fruhauf, J., Schulz, M., Chiwora, F.M., Volz, J., and Becker, K. (2000) Riboflavin deficiency and preeclampsia. Obstet Gynecol 96: 38–44.
81. Wels, M., Francke, C., Kerkhoven, R., Kleerebezem, M., and Siezen, R.J. (2006) Predicting cisacting elements of Lactobacillus plantarum by comparative genomics with different taxonomic subgroups. Nucleic Acids Res 34: 1947–1958.
82. Wilson, J.A. (1983) Disorders of vitamins: deficiency, excess and errors of metabolism. In Harrison's Principles of Internal Medicine. Petersdorf, R.G., and Harrison, T.R. (eds). New York, NY, USA: McGraw-Hill Book, pp. 461–470.
83. Wrong, O.M., Edmonds, C.J., and Chadwich, V.S. (1981) The Large Intestine; its Role in Mammalian Nutrition and Homeostasis. New York, NY, USA: Wiley & Sons.