Folate-producing bifidobacteria: metabolism, genetics, and relevance

Maria Rosaria D’Aimmo , Maria Satti , Donatella Scarafile , Monica Modesto , Stefano Pascarelli , Simone Andrea Biagini , Donata Luiselli , Paola Mattarelli , Thomas Andlid

Microbiome Research Reports ›› 2023, Vol. 3 ›› Issue (1) : 11

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Microbiome Research Reports ›› 2023, Vol. 3 ›› Issue (1) :11 DOI: 10.20517/mrr.2023.59
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Folate-producing bifidobacteria: metabolism, genetics, and relevance

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Abstract

Folate (the general term for all bioactive forms of vitamin B9) plays a crucial role in the evolutionary highly conserved one-carbon (1C) metabolism, a network including central reactions such as DNA and protein synthesis and methylation of macromolecules. Folate delivers 1C units, such as methyl and formyl, between reactants. Plants, algae, fungi, and many bacteria can naturally produce folate, whereas animals, including humans, must obtain folate from external sources. For humans, folate deficiency is, however, a widespread problem. Bifidobacteria constitute an important component of human and many animal microbiomes, providing various health advantages to the host, such as producing folate. This review focuses on bifidobacteria and folate metabolism and the current knowledge of the distribution of genes needed for complete folate biosynthesis across different bifidobacterial species. Biotechnologies based on folate-trophic probiotics aim to create fermented products enriched with folate or design probiotic supplements that can synthesize folate in the colon, improving overall health. Therefore, bifidobacteria (alone or in association with other microorganisms) may, in the future, contribute to reducing widespread folate deficiencies prevalent among vulnerable human population groups, such as older people, women at child-birth age, and people in low-income countries.

Keywords

Bifidobacteria / folate metabolism / folate biofortification / gut microbiota

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Maria Rosaria D’Aimmo, Maria Satti, Donatella Scarafile, Monica Modesto, Stefano Pascarelli, Simone Andrea Biagini, Donata Luiselli, Paola Mattarelli, Thomas Andlid. Folate-producing bifidobacteria: metabolism, genetics, and relevance. Microbiome Research Reports, 2023, 3(1): 11 DOI:10.20517/mrr.2023.59

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References

[1]

Blakley RL.Nomenclature and symbols for folic acid and related compounds.Eur J Biochem1987;168:251-3

[2]

Scaglione F.Folate, folic acid and 5-methyltetrahydrofolate are not the same thing.Xenobiotica2014;44:480-8

[3]

de Giori GS, Leblanc JG. Chapter 2 - folate production by lactic acid bacteria. In: Watson RR, Preedy VR, Zibadi S, editors. Polyphenols: prevention and treatment of human disease. Elsevier; 2018. pp. 15-29.

[4]

Katan MB,Connor WE.Which are the greatest recent discoveries and the greatest future challenges in nutrition?.Eur J Clin Nutr2009;63:2-10

[5]

LeBlanc JG,de Giori GS,van Sinderen D.Bacteria as vitamin suppliers to their host: a gut microbiota perspective.Curr Opin Biotechnol2013;24:160-8

[6]

Mosley BS,Siega-Riz AM.National Birth Defects Prevention StudyNeural tube defects and maternal folate intake among pregnancies conceived after folic acid fortification in the United States.Am J Epidemiol2009;169:9-17 PMCID:PMC3139973

[7]

Hjortmo S,Jastrebova J.Inherent biodiversity of folate content and composition in yeasts.Trends Food Sci Technol2005;16:311-6

[8]

Lattof SR,Moran AC.Developing measures for WHO recommendations on antenatal care for a positive pregnancy experience: a conceptual framework and scoping review.BMJ Open2019;9:e024130 PMCID:PMC6502222

[9]

Fan G,Liu Q.Association of maternal folic acid supplementation during pregnancy with newborn telomere length.Reprod Toxicol2022;114:52-6

[10]

Pieroth R,Day S.Folate and its impact on cancer risk.Curr Nutr Rep2018;7:70-84 PMCID:PMC6132377

[11]

Panel on Dietetic Products, Nutrition and Allergies (NDA). Scientific opinion on dietary reference values for folate.EFSA J2014;12:3893

[12]

Hjortmo S,Jastrebova J.Biofortification of folates in white wheat bread by selection of yeast strain and process.Int J Food Microbiol2008;127:32-6

[13]

Wong CB,Odamaki T.Different physiological properties of human-residential and non-human-residential bifidobacteria in human health.Benef Microbes2018;9:111-22

[14]

Patring JDM,Jastrebova JA,Andlid TA.Characterization and quantification of folates produced by yeast strains isolated from kefir granules.Eur Food Res Technol2006;223:633-7

[15]

Hjortmo SB,Andlid TA.Production of folates by yeasts in Tanzanian fermented togwa.FEMS Yeast Res2008;8:781-7

[16]

Wills L.Treatment of “pernicious anaemia of pregnancy” and “tropical anaemia”.Br Med J1931;1:1059-64 PMCID:PMC2314785

[17]

Mitchell HK,Williams RJ.The concentration of “folic acid”.J Am Chem Soc1941;63:2284

[18]

Burg AW.The biosynthesis of folic acid. VIII. Purification and properties of the enzyme that catalyzes the production of formate from carbon atom 8 of guanosine triphosphate.J Biol Chem1968;243:2349-58

[19]

Richey DP.The biosynthesis of folic acid. IX. Purification and properties of the enzymes required for the formation of dihydropteroic acid.J Biol Chem1969;244:1582-92

[20]

Shiota T,Jackson R.The enzymatic synthesis of hydroxymethyldihydropteridine pyrophosphate and dihydrofolate.Biochemistry1969;8:5022-8

[21]

Brown GM.The biosynthesis of pteridines.Adv Enzymol Relat Areas Mol Biol1971;35:35-77

[22]

Gregory J.Vitamins. In: Damodaran S, Parkin KL, eds. Food chemistry. CRC Press; 2017. pp. 543-626.

[23]

Hasan T,Bansal AK,Sharma GS.Disturbed homocysteine metabolism is associated with cancer.Exp Mol Med2019;51:1-13 PMCID:PMC6389897

[24]

Fowler B.The folate cycle and disease in humans.Kidney Int Suppl2001;78:S221-9

[25]

Friedrich W. Folic acid and unconjugates pteridines (Chaper 10). In: De Gruyter W, editor. Vitamins. Berlin: De Gruyter; 1988. pp. 619-752. Available from: https://books.google.it/books?id=VS9YWqnMpNsC&printsec=frontcover&hl=it&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false. [Last accessed on 11 Dec 2023]

[26]

Qiu A,Sakaris A.Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption.Cell2006;127:917-28

[27]

Wan Q,Wilson MA.Toward resolving the catalytic mechanism of dihydrofolate reductase using neutron and ultrahigh-resolution X-ray crystallography.Proc Natl Acad Sci U S A2014;111:18225-30 PMCID:PMC4280638

[28]

Gregory JF 3rd,Liao JF,Toth JP.Kinetic model of folate metabolism in nonpregnant women consuming [2H2]folic acid: isotopic labeling of urinary folate and the catabolite para-acetamidobenzoylglutamate indicates slow, intake-dependent, turnover of folate pools.J Nutr1998;128:1896-906

[29]

Herbert V.The 1986 Herman award lecture. Nutrition science as a continually unfolding story: the folate and vitamin B-12 paradigm.Am J Clin Nutr1987;46:387-402

[30]

Ohrvik VE.Human folate bioavailability.Nutrients2011;3:475-90 PMCID:PMC3257685

[31]

Bailey LB. Folate in health and disease. CRC Press; 1995. pp. 1-22. Available from: http://repository.universitasbumigora.ac.id/862/732/216%20Folate%20in%20Health%20and%20Disease%2C%20Second%20Edition%20%20%28%20PDFDrive%20%29.pdf. [Last accessed on 4 Dec 2023]

[32]

Laanpere M,Stavreus-Evers A,Yngve A.Folate-mediated one-carbon metabolism and its effect on female fertility and pregnancy viability.Nutr Rev2010;68:99-113

[33]

Shane B.Transport and metabolism of folates by bacteria.J Biol Chem1975;250:2243-53

[34]

Zhao R,Wang Y,Low PS.A role for the proton-coupled folate transporter (PCFT-SLC46A1) in folate receptor-mediated endocytosis.J Biol Chem2009;284:4267-74 PMCID:PMC2640977

[35]

Ducker GS.One-carbon metabolism in health and disease.Cell Metab2017;25:27-42 PMCID:PMC5353360

[36]

Wagner C.Biochemical role of folate in cellular metabolism.Clin Res Regul Aff2001;18:161-80

[37]

Lucock M.Folic acid: nutritional biochemistry, molecular biology, and role in disease processes.Mol Genet Metab2000;71:121-38

[38]

Jägerstad M.Occurrence, stability, and determination of formyl folates in foods.J Agric Food Chem2013;61:9758-68

[39]

Strandler HS,Jägerstad M.Challenges in the determination of unsubstituted food folates: impact of stabilities and conversions on analytical results.J Agric Food Chem2015;63:2367-77

[40]

De Brouwer V,Van De Steene JC.Optimisation and validation of a liquid chromatography-tandem mass spectrometry method for folates in rice.J Chromatogr A2008;1215:125-32

[41]

Matella NJ,Gregory JF 3rd.Capillary electrophoresis and high-performance liquid chromatography determination of polyglutamyl 5-methyltetrahydrofolate forms in citrus products.J Agric Food Chem2005;53:2268-74

[42]

Dang J.Folate retention in selected processed legumes.Food Chem2000;68:295-8

[43]

McKillop DJ,Daly D.The effect of different cooking methods on folate retention in various foods that are amongst the major contributors to folate intake in the UK diet.Br J Nutr2002;88:681-8

[44]

Horne DW.High-performance liquid chromatographic measurement of 5,10-methylenetetrahydrofolate in liver.Anal Biochem2001;297:154-9

[45]

O’Broin JD,Brown JP.Nutritional stability of various naturally occurring monoglutamate derivatives of folic acid.Am J Clin Nutr1975;28:438-44

[46]

Forssén KM,Wigertz K.Folates and dairy products: a critical update.J Am Coll Nutr2000;19:100S-10S

[47]

Scott J,Fletcher J.Folic acid and folates: the feasibility for nutritional enhancement in plant foods.J Sci Food Agric2000;80:795-824

[48]

Andlid TA,Jastrebova J.Folate and bifidobacteria. In: Mattarelli P, Biavati B, Holzapfel WH, Wood BJB, editors. The bifidobacteria and related organisms. Academic Press; 2018. pp. 195-212

[49]

Arcot J.Folate: methods of analysis.Trends Food Sci Technol2005;16:253-66

[50]

Patring JD,Hjortmo SB,Jägerstad IM.Development of a simplified method for the determination of folates in baker’s yeast by HPLC with ultraviolet and fluorescence detection.J Agric Food Chem2005;53:2406-11

[51]

Scorrano G,Vetro DL.Genomic ancestry, diet and microbiomes of Upper Palaeolithic hunter-gatherers from San Teodoro cave.Commun Biol2022;5:1262 PMCID:PMC9674856

[52]

Sender R,Milo R.Revised estimates for the number of human and bacteria cells in the body.PLoS Biol2016;14:e1002533 PMCID:PMC4991899

[53]

Hou K,Chen XY.Microbiota in health and diseases.Signal Transduct Target Ther2022;7:135 PMCID:PMC9034083

[54]

Rinninella E,Cintoni M.What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases.Microorganisms2019;7:14 PMCID:PMC6351938

[55]

Goodrich JK,Poole AC.Human genetics shape the gut microbiome.Cell2014;159:789-99 PMCID:PMC4255478

[56]

Turnbaugh PJ,Faith JJ,Knight R.The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.Sci Transl Med2009;1:6ra14 PMCID:PMC2894525

[57]

Zhernakova A,Bonder MJ.Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity.Science2016;352:565-9 PMCID:PMC5240844

[58]

D’Aimmo MR,Mattarelli P,Andlid T.Biosynthesis and cellular content of folate in bifidobacteria across host species with different diets.Anaerobe2014;30:169-77

[59]

Asrar FM.Bacterially synthesized folate and supplemental folic acid are absorbed across the large intestine of piglets.J Nutr Biochem2005;16:587-93

[60]

Kim TH,Darling PB.A large pool of available folate exists in the large intestine of human infants and piglets.J Nutr2004;134:1389-94

[61]

Thomas CM,Spinler JK.FolC2-mediated folate metabolism contributes to suppression of inflammation by probiotic Lactobacillus reuteri.Microbiologyopen2016;5:802-18 PMCID:PMC5061717

[62]

Meucci A,Zago M.Folates biosynthesis by Streptococcus thermophilus during growth in milk.Food Microbiol2018;69:116-22

[63]

Said HM.Intestinal absorption of water-soluble vitamins: an update.Curr Opin Gastroenterol2006;22:140-6

[64]

LeBlanc JG,del Valle MJ.B-group vitamin production by lactic acid bacteria--current knowledge and potential applications.J Appl Microbiol2011;111:1297-309

[65]

Rossi M,Raimondi S.Folate production by probiotic bacteria.Nutrients2011;3:118-34 PMCID:PMC3257725

[66]

Mosso AL,Motta C,Ribotta P.Effect of fermentation in nutritional, textural and sensorial parameters of vegan-spread products using a probiotic folate-producing Lactobacillus sakei strain.LWT2020;127:109339

[67]

Deguchi Y,Mutai M.Comparative studies on synthesis of water-soluble vitamins among human species of bifidobacteria.Agric Biol Chem1985;49:13-9

[68]

de Bree A, van Dusseldorp M, Brouwer IA, van het Hof KH, Steegers-Theunissen RP. Folate intake in Europe: recommended, actual and desired intake.Eur J Clin Nutr1997;51:643-60

[69]

White RH.Purine biosynthesis in the domain Archaea without folates or modified folates.J Bacteriol1997;179:3374-7 PMCID:PMC179124

[70]

Engevik MA,Röth D.Microbial metabolic capacity for intestinal folate production and modulation of host folate receptors.Front Microbiol2019;10:2305 PMCID:PMC6795088

[71]

Magnúsdóttir S,de Crécy-Lagard V.Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes.Front Genet2015;6:148 PMCID:PMC4403557

[72]

Alessandri G,Ventura M.The genus Bifidobacterium: from genomics to functionality of an important component of the mammalian gut microbiota.Comput Struct Biotechnol J2021;19:1472-87 PMCID:PMC7979991

[73]

Michelini S,Oki K.Isolation and identification of cultivable Bifidobacterium spp. from the faeces of 5 baby common marmosets (Callithrix jacchus L.).Anaerobe2015;33:101-4

[74]

D’Aimmo MR,Biavati B,Andlid T.The potential of bifidobacteria as a source of natural folate.J Appl Microbiol2012;112:975-84

[75]

Filannino P,De Angelis M.Hydroxycinnamic acids used as external acceptors of electrons: an energetic advantage for strictly heterofermentative lactic acid bacteria.Appl Environ Microbiol2014;80:7574-82 PMCID:PMC4249242

[76]

Rossi M,Costantino L.Folate: relevance of chemical and microbial production. In: Vandamme EJ, Revuelta JL, editors. Industrial biotechnology of vitamins, biopigments, and antioxidants. Wiley; 2016. pp. 103-28.

[77]

Czarnowska-Kujawska M.Changes in the folate content and fatty acid profile in fermented milk produced with different starter cultures during storage.Molecules2021;26:6063 PMCID:PMC8512886

[78]

Malinowska AM,Kok DE.Ex vivo folate production by fecal bacteria does not predict human blood folate status: associations between dietary patterns, gut microbiota, and folate metabolism.Food Res Int2022;156:111290

[79]

Aufreiter S. Folate absorption across the colon and the modulation of bacterial folate synthesis by diet. Available from: https://tspace.library.utoronto.ca/bitstream/1807/32926/1/Aufreiter_Susanne_201006_PhD_thesis.pdf. [Last accessed on 4 Dec 2023]

[80]

Laiño JE,Savoy de Giori G.Development of a high folate concentration yogurt naturally bio-enriched using selected lactic acid bacteria.LWT Food Sci Technol2013;54:1-5

[81]

Laiño JE,de Moreno de LeBlanc A,LeBlanc JG.Characterization of folate production and probiotic potential of Streptococcus gallolyticus subsp.macedonicus2019;79:20-6

[82]

Pompei A,Amaretti A,Matteuzzi D.Folate production by bifidobacteria as a potential probiotic property.Appl Environ Microbiol2007;73:179-85 PMCID:PMC1797147

[83]

Nordberg H,Dusheyko S.The genome portal of the Department of Energy Joint Genome Institute: 2014 updates.Nucleic Acids Res2014;42:D26-31 PMCID:PMC3965075

[84]

Dehal PS,Price MN.MicrobesOnline: an integrated portal for comparative and functional genomics.Nucleic Acids Res2010;38:D396-400 PMCID:PMC2808868

[85]

Modesto M,Stefanini I.Bifidobacterium lemurum sp. nov., from faeces of the ring-tailed lemur (Lemur catta).Int J Syst Evol Microbiol2015;65:1726-34

[86]

Modesto M,Oki K,Watanabe K.Bifidobacterium catulorum sp. nov., a novel taxon from the faeces of the baby common marmoset (Callithrix jacchus).Int J Syst Evol Microbiol2018;68:575-81

[87]

Duranti S,Napoli S.Characterization of the phylogenetic diversity of five novel species belonging to the genus Bifidobacterium: Bifidobacterium castoris sp. nov., Bifidobacterium callimiconis sp. nov., Bifidobacterium goeldii sp. nov., Bifidobacterium samirii sp. nov. and Bifidobacterium dolichotidis sp. nov.Int J Syst Evol Microbiol2019;69:1288-98

[88]

Milani C,Duranti S.Genomic encyclopedia of type strains of the genus Bifidobacterium.Appl Environ Microbiol2014;80:6290-302 PMCID:PMC4178644

[89]

Sugahara H,Hashikura N,Xiao JZ.Differences in folate production by bifidobacteria of different origins.Biosci Microbiota Food Health2015;34:87-93 PMCID:PMC4654071

[90]

Ley RE,Lozupone C.Evolution of mammals and their gut microbes.Science2008;320:1647-51 PMCID:PMC2649005

[91]

Pompei A,Amaretti A.Administration of folate-producing bifidobacteria enhances folate status in Wistar rats.J Nutr2007;137:2742-46

[92]

Strozzi GP.Quantification of folic acid in human feces after administration of Bifidobacterium probiotic strains.J Clin Gastroenterol2008;42:179-84

[93]

Mason JB,Jacques PF.A temporal association between folic acid fortification and an increase in colorectal cancer rates may be illuminating important biological principles: a hypothesis.Cancer Epidemiol Biomarkers Prev2007;16:1325-9

[94]

Hirsch S,Albala C.Colon cancer in Chile before and after the start of the flour fortification program with folic acid.Eur J Gastroenterol Hepatol2009;21:436-9

[95]

Albuquerque MAC,Bedani R,Saad SMI.Influence of passion fruit by-product and fructooligosaccharides on the viability of Streptococcus thermophilus TH-4 and Lactobacillus rhamnosus LGG in folate bio-enriched fermented soy products and their effect on probiotic survival and folate bio-accessibility under in vitro simulated gastrointestinal conditions.Int J Food Microbiol2019;292:126-36

[96]

Albuquerque MA,Vieira AD,Saad SM.Supplementation with fruit and okara soybean by-products and amaranth flour increases the folate production by starter and probiotic cultures.Int J Food Microbiol2016;236:26-32

[97]

Greppi A,Botta C,Guyot JP.Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food.Food Microbiol2017;62:169-77

[98]

Korhola M,Juuti K.Production of folate in oat bran fermentation by yeasts isolated from barley and diverse foods.J Appl Microbiol2014;117:679-89

[99]

Saubade F,Guyot JP.Lactic acid fermentation as a tool for increasing the folate content of foods.Crit Rev Food Sci Nutr2017;57:3894-910

[100]

Turpin W,Guyot JP.Genetic screening of functional properties of lactic acid bacteria in a fermented pearl millet slurry and in the metagenome of fermented starchy foods.Appl Environ Microbiol2011;77:8722-34 PMCID:PMC3233104

[101]

Crittenden RG,Playne MJ.Synthesis and utilisation of folate by yoghurt starter cultures and probiotic bacteria.Int J Food Microbiol2003;80:217-22

[102]

Lin MY.Folate levels in cultures of lactic acid bacteria.Int Dairy J2000;10:409-13Available from: https://www.sciencedirect.com/science/article/abs/pii/S095869460000056X. [Last accessed on 6 Dec 2023]

[103]

Holasová M,Roubal P.biosynthesis of folates by lactic acid bacteria and propionibacteria in fermented milk.Czech J Food Sci2004;22:175-81

[104]

Capozzi V,Dueñas MT,Spano G.Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products.Appl Microbiol Biotechnol2012;96:1383-94

[105]

Hjortmo S,Andlid T.Growth rate and medium composition strongly affect folate content in Saccharomyces cerevisiae.Int J Food Microbiol2008;123:93-100

[106]

Sauer M,Valli M.Production of L-ascorbic acid by metabolically engineered Saccharomyces cerevisiae and Zygosaccharomyces bailii.Appl Environ Microbiol2004;70:6086-91 PMCID:PMC522139

[107]

Rosa JCC,Alvim MCT,Van Dijck P.Metabolic engineering of Kluyveromyces lactis for L-ascorbic acid (vitamin C) biosynthesis.Microb Cell Fact2013;12:59 PMCID:PMC3699391

[108]

Fang H,Zhang D.Microbial production of vitamin B12: a review and future perspectives.Microb Cell Fact2017;16:15 PMCID:PMC5282855

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