Microbial Metabolic Capacity for Intestinal Folate Production and Modulation of Host Folate Receptors

Frontiers in Microbiology

Volumn 10, Issue , 2019, Pages

  Engevik, Melinda A ^a,b   Morra, Christina N ^a   Röth, Daniel ^c   Engevik, Kristen ^a   Spinler, Jennifer K ^a,b   Devaraj, Sridevi ^a,b   Crawford, Sue E ^a   Estes, Mary K ^a   Kalkum, Markus ^c   Versalovic, James ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

B vitamin; enteroids; folate transporters; folylpolyglutamate; Lactobacilli; Lactobacillus reuteri; microbiome

Indexed keywords

BACTERIAL RNA; FOLATE RECEPTOR; GENOMIC DNA; PROTON COUPLED FOLATE TRANSPORTER; PTEROPTIN; REDUCED FOLATE CARRIER; VITAMIN B COMPLEX;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOSYNTHESIS; COHORT ANALYSIS; COLON TISSUE; COLONY FORMING UNIT; COMPARATIVE STUDY; CONTROLLED STUDY; DNA SYNTHESIS; EPIGENETICS; EVALUATION STUDY; GENE EXPRESSION; GENOME ANALYSIS; GROWTH CURVE; HOST MICROBE INTERACTION; HUMAN; HUMAN TISSUE; IMAGE GUIDED BIOPSY; IMMUNOMODULATION; INTESTINE FLORA; LACTOBACILLUS REUTERI; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLIC CAPACITY; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; UPREGULATION;

EID: 85074175085     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2019.02305     Document Type: Article

References (118)

1. Adams M. R., Marteau P., (1995). On the safety of lactic acid bacteria from food. Int. J. Food Microbiol. 27 263–264.
2. Askari B. S., Krajinovic M., (2010). Dihydrofolate reductase gene variations in susceptibility to disease and treatment outcomes. Curr. Genomics 11 578–583. 10.2174/138920210793360925 21629435
3. Asrar F. M., O’Connor D. L., (2005). Bacterially synthesized folate and supplemental folic acid are absorbed across the large intestine of piglets. J. Nutr. Biochem. 16 587–593. 10.1016/j.jnutbio.2005.02.006 16081276
4. Aufreiter S., Gregory J. F., III Pfeiffer C. M., Fazili Z., Kim Y. I., Marcon N., (2009). Folate is absorbed across the colon of adults: evidence from cecal infusion of (13)C-labeled [6S]-5-formyltetrahydrofolic acid. Am. J. Clin. Nutr. 90 116–123. 10.3945/ajcn.2008.27345 19439459
5. Baccouri O., Boukerb A. M., Farhat L. B., Zebre A., Zimmermann K., Domann E., (2019). Probiotic potential and safety evaluation of Enterococcus faecalis OB14 and OB15, isolated from traditional tunisian testouri cheese and rigouta, using physiological and genomic analysis. Front. Microbiol. 10:881. 10.3389/fmicb.2019.00881 31105672
6. Baggott J. E., Tamura T., (2015). Folate-dependent purine nucleotide biosynthesis in humans. Adv. Nutr. 6 564–571. 10.3945/an.115.008300 26374178
7. Balashova O. A., Visina O., Borodinsky L. N., (2018). Folate action in nervous system development and disease. Dev. Neurobiol. 78 391–402. 10.1002/dneu.22579 29380544
8. Barber R. C., Lammer E. J., Shaw G. M., Greer K. A., Finnell R. H., (1999). The role of folate transport and metabolism in neural tube defect risk. Mol. Genet. Metab. 66 1–9. 10.1006/mgme.1998.2787 9973541
9. Berding K., Donovan S. M., (2016). Microbiome and nutrition in autism spectrum disorder: current knowledge and research needs. Nutr. Rev. 74 723–736. 10.1093/nutrit/nuw048 27864534
10. Bhandari S. D., Gregory J. F., III (1992). Folic acid, 5-methyl-tetrahydrofolate and 5-formyl-tetrahydrofolate exhibit equivalent intestinal absorption, metabolism and in vivo kinetics in rats. J. Nutr. 122 1847–1854. 10.1093/jn/122.9.1847 1512634
11. Birnbaum J., Pai C. H., Lichstein H. C., (1967). Biosynthesis of biotin in microorganisms. V. Control of vitamer production. J. Bacteriol. 94 1846–1853. 4965364
12. Blakley R. L., Benkovic S. J., (1984). Folates and Pterins. New York, NJ: Wiley.
13. Blom H. J., Shaw G. M., den Heijer M., Finnell R. H., (2006). Neural tube defects and folate: case far from closed. Nat. Rev. Neurosci. 7 724–731. 10.1038/nrn1986 16924261
14. Blutt S. E., Crawford S. E., Ramani S., Zou W. Y., Estes M. K., (2018). Engineered human gastrointestinal cultures to study the microbiome and infectious diseases. Cell. Mol. Gastroenterol. Hepatol. 5 241–251. 10.1016/j.jcmgh.2017.12.001 29675450
15. Britton R. A., Irwin R., Quach D., Schaefer L., Zhang J., Lee T., (2014). Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J. Cell Physiol. 229 1822–1830. 10.1002/jcp.24636 24677054
16. Brosnan M. E., MacMillan L., Stevens J. R., Brosnan J. T., (2015). Division of labour: how does folate metabolism partition between one-carbon metabolism and amino acid oxidation? Biochem. J. 472 135–146. 10.1042/BJ20150837 26567272
17. Burgess C. M., Smid E. J., Rutten G., van Sinderen D., (2006). A general method for selection of riboflavin-overproducing food grade micro-organisms. Microb. Cell Fact. 5:24. 10.1186/1475-2859-5-24 16848883
18. Camilo E., Zimmerman J., Mason J. B., Golner B., Russell R., Selhub J., (1996). Folate synthesized by bacteria in the human upper small intestine is assimilated by the host. Gastroenterology 110 991–998. 8613033
19. Chave K. J., Ryan T. J., Chmura S. E., Galivan J., (2003). Identification of single nucleotide polymorphisms in the human gamma-glutamyl hydrolase gene and characterization of promoter polymorphisms. Gene 319 167–175. 14597182
20. Clevers H., (2016). Modeling development and disease with organoids. Cell 165 1586–1597. 10.1016/j.cell.2016.05.082 27315476
21. Crittenden R. G., Martinez N. R., Playne M. J., (2003). Synthesis and utilisation of folate by yoghurt starter cultures and probiotic bacteria. Int. J. Food Microbiol. 80 217–222. 12423923
22. Cummings J. H., Macfarlane G. T., (1997). Role of intestinal bacteria in nutrient metabolism. JPEN J. Parenter. Enteral Nutr. 21 357–365. 10.1177/0148607197021006357 9406136
23. D’Argenio V., Salvatore F., (2015). The role of the gut microbiome in the healthy adult status. Clin. Chim. Acta 451(Pt A), 97–102. 10.1016/j.cca.2015.01.003 25584460
24. Das P., Babaei P., Nielsen J., (2019). Metagenomic analysis of microbe-mediated vitamin metabolism in the human gut microbiome. BCM Genomics 20 208–219. 10.1186/s12864-019-5591-7 30866812
25. Engevik M. A., Aihara E., Montrose M. H., Shull G. E., Hassett D. J., Worrell R. T., (2013). Loss of NHE3 alters gut microbiota composition and influences Bacteroides thetaiotaomicron growth. Am. J. Physiol. Gastrointest. Liver Physiol. 305 G697–G711. 10.1152/ajpgi.00184.2013 24072680
26. Engevik M. A., Engevik K. A., Yacyshyn M. B., Wang J., Hassett D. J., Darien B., (2015). Human Clostridium difficile infection: inhibition of NHE3 and microbiota profile. Am. J. Physiol. Gastrointest. Liver Physiol. 308 G497–G509. 10.1152/ajpgi.00090.2014 25552580
27. Ettayebi K., Crawford S. E., Murakami K., Broughman J. R., Karandikar U., Tenge V. R., (2016). Replication of human noroviruses in stem cell-derived human enteroids. Science 353 1387–1393. 10.1126/science.aaf5211 27562956
28. Evans D. F., Pye G., Bramley R., Clark A. G., Dyson T. J., Hardcastle J. D., (1988). Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29 1035–1041. 3410329
29. Fatheree N. Y., Liu Y., Taylor C. M., Hoang T. K., Cai C., Rahbar M. H., (2017). Lactobacillus reuteri for infants with colic: a double-blind, placebo-controlled, randomized clinical trial. J. Pediatr. 191 170.e2–178.e2. 10.1016/j.jpeds.2017.07.036 28969890
30. Ferstl R., Frei R., Schiavi E., Konieczna P., Barcik W., Ziegler M., (2014). Histamine receptor 2 is a key influence in immune responses to intestinal histamine-secreting microbes. J. Allergy Clin. Immunol. 134 744–746e743. 10.1016/j.jaci.2014.04.034 24954261
31. Finkbeiner S. R., Zeng X. L., Utama B., Atmar R. L., Shroyer N. F., Estes M. K., (2012). Stem cell-derived human intestinal organoids as an infection model for rotaviruses. mBio 3:e00159-12. 10.1128/mBio.00159-12 22761392
32. Foulke-Abel J., In J., Kovbasnjuk O., Zachos N. C., Ettayebi K., Blutt S. E., (2014). Human enteroids as an ex-vivo model of host-pathogen interactions in the gastrointestinal tract. Exp. Biol. Med. 239 1124–1134. 10.1177/1535370214529398 24719375
33. Foulke-Abel J., In J., Yin J., Zachos N. C., Kovbasnjuk O., Estes M. K., (2016). Human enteroids as a model of upper small intestinal ion transport physiology and pathophysiology. Gastroenterology 150 638.e8–649.e8. 10.1053/j.gastro.2015.11.047 26677983
34. Frei R., Ferstl R., Konieczna P., Ziegler M., Simon T., Rugeles T. M., (2013). Histamine receptor 2 modifies dendritic cell responses to microbial ligands. J. Allergy Clin. Immunol. 132 194–204. 10.1016/j.jaci.2013.01.013 23465664
35. Friend B. A., Fiedler J. M., Shahani K. M., (1983). Influence of culture selection on the flavor, antimicrobial activity, β-galactosidase and B-vitamins of yoghurt. Milchwissenschaft 38 133–136.
36. Galofre M., Palao D., Vicario M., Nart J., Violant D., (2018). Clinical and microbiological evaluation of the effect of Lactobacillus reuteri in the treatment of mucositis and peri-implantitis: a triple-blind randomized clinical trial. J. Periodontal Res. 53 378–390. 10.1111/jre.12523 29352461
37. Gronbach K., Eberle U., Muller M., Olschlager T. A., Dobrindt U., Leithauser F., (2010). Safety of probiotic Escherichia coli strain Nissle 1917 depends on intestinal microbiota and adaptive immunity of the host. Infect. Immun. 78 3036–3046. 10.1128/IAI.00218-0 20421387
38. Hague A., Elder D. J., Hicks D. J., Paraskeva C., (1995). Apoptosis in colorectal tumour cells: induction by the short chain fatty acids butyrate, propionate and acetate and by the bile salt deoxycholate. Int. J. Cancer 60 400–406. 7829251
39. Hayakawa K., Kimura M., Kasaha K., Matsumoto K., Sansawa H., Yamori Y., (2004). Effect of a gamma-aminobutyric acid-enriched dairy product on the blood pressure of spontaneously hypertensive and normotensive Wistar-Kyoto rats. Br. J. Nutr. 92 411–417. 15469644
40. Hiraoka M., Kagawa Y., (2017). Genetic polymorphisms and folate status. Cong. Anom. 57 142–149. 10.1111/cga.12232 28598562
41. Hollister E. B., Gao C., Versalovic J., (2014). Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 146 1449–1458. 10.1053/j.gastro.2014.01.052 24486050
42. Hugenholtz J., Smid E. J., (2002). Nutraceutical production with food-grade microorganisms. Curr. Opin. Biotechnol. 13 497–507. 12459344
43. Ichihashi T., Takagishi Y., Uchida K., Yamada H., (1992). Colonic absorption of menaquinone-4 and menaquinone-9 in rats. J. Nutr. 122 506–512. 10.1093/jn/122.3.506 1542008
44. Izquierdo Canas P. M., Gomez Alonso S., Ruiz Perez P., Sesena Prieto S., Garcia Romero E., Palop Herreros M. L., (2009). Biogenic amine production by Oenococcus oeni isolates from malolactic fermentation of Tempranillo wine. J. Food Prot. 72 907–910. 19435249
45. Jayashree S., Jayaraman K., Kalaichelvan G., (2010). Isolation, screening and characterization of riboflavin producing lactic acid bacteria from Katpadi, Vellore district. Recent Res. Sci. Technol. 2 83–88.
46. Jensen H., Roos S., Jonsson H., Rud I., Grimmer S., van Pijkeren J. P., (2014). Role of Lactobacillus reuteri cell and mucus-binding protein A (CmbA) in adhesion to intestinal epithelial cells and mucus in vitro. Microbiology 160(Pt 4), 671–681. 10.1099/mic.0.073551-0 24473252
47. Kaehler S. T., Baumgartner H., Jeske M., Anliker M., Schennach H., Marschang P., (2012). Prevalence of hypovitaminosis D and folate deficiency in healthy young female Austrian students in a health care profession. Eur. J. Nutr. 51 1021–1031. 10.1007/s00394-011-0281-5 22116202
48. Kamen B. A., Smith A. K., (2004). A review of folate receptor alpha cycling and 5-methyltetrahydrofolate accumulation with an emphasis on cell models in vitro. Adv. Drug Deliv. Rev. 56 1085–1097. 10.1016/j.addr.2004.01.002 15094208
49. Kanehisa M., Goto S., (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28 27–30. 10592173
50. KEGG (2017). Folate Biosynthesis Reference Pathway. Tokyo: Kanehisa Laboratories.
51. Kemperman R. F., Veurink M., van der Wal T., Knegtering H., Bruggeman R., Fokkema M. R., (2006). Low essential fatty acid and B-vitamin status in a subgroup of patients with schizophrenia and its response to dietary supplementation. Prostaglandins Leukot. Essent. Fatty Acids 74 75–85. 10.1016/j.plefa.2005.11.004 16384692
52. Kibe R., Kurihara S., Sakai Y., Suzuki H., Ooga T., Sawaki E., (2014). Upregulation of colonic luminal polyamines produced by intestinal microbiota delays senescence in mice. Sci. Rep. 4:4548. 10.1038/srep04548 24686447
53. Kim D. H., Ahn Y. O., Lee B. H., Tsuji E., Kiyohara C., Kono S., (2004). Methylenetetrahydrofolate reductase polymorphism, alcohol intake, and risks of colon and rectal cancers in Korea. Cancer Lett. 216 199–205. 10.1016/j.canlet.2004.08.014 15533596
54. Kim T. H., Yang J., Darling P. B., O’Connor D. L., (2004). A large pool of available folate exists in the large intestine of human infants and piglets. J. Nutr. 134 1389–1394. 10.1093/jn/134.6.1389 15173401
55. Kim Y. I., (1999). Folate and cancer prevention: a new medical application of folate beyond hyperhomocysteinemia and neural tube defects. Nutr. Rev. 57 314–321. 10575908
56. Kim Y. I., (2006). Does a high folate intake increase the risk of breast cancer? Nutr. Rev. 64(10 Pt 1), 468–475. 17063929
57. Kimura M., Hayakawa K., Sansawa H., (2002). Involvement of gamma-aminobutyric acid (GABA) B receptors in the hypotensive effect of systemically administered GABA in spontaneously hypertensive rats. Jpn. J. Pharmacol. 89 388–394. 12233817
58. Kumar C. K., Moyer M. P., Dudeja P. K., Said H. M., (1997). A protein-tyrosine kinase-regulated, pH-dependent, carrier-mediated uptake system for folate in human normal colonic epithelial cell line NCM460. J. Biol. Chem. 272 6226–6231. 9045638
59. Lakoff A., Fazili Z., Aufreiter S., Pfeiffer C. M., Connolly B., Gregory J. F., (2014). Folate is absorbed across the human colon: evidence by using enteric-coated caplets containing 13C-labeled [6S]-5-formyltetrahydrofolate. Am. J. Clin. Nutr. 100 1278–1286. 10.3945/ajcn.114.091785 25332326
60. LeBlanc J. G., Aubry C., Cortes-Perez N. G., de Moreno de LeBlanc A., Vergnolle N., Langella P., (2013a). Mucosal targeting of therapeutic molecules using genetically modified lactic acid bacteria: an update. FEMS Microbiol. Lett. 344 1–9. 10.1111/1574-6968.12159 23600579
61. LeBlanc J. G., Milani C., de Giori G. S., Sesma F., van Sinderen D., Ventura M., (2013b). Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr. Opin. Biotechnol. 24 160–168. 10.1016/j.copbio.2012.08.005 22940212
62. LeBlanc J. G., Laino J. E., del Valle M. J., Vannini V., van Sinderen D., Taranto M. P., (2011). B-group vitamin production by lactic acid bacteria–current knowledge and potential applications. J. Appl. Microbiol. 111 1297–1309. 10.1111/j.1365-2672.2011.05157.x 21933312
63. Luk B., Veeraragavan S., Engevik M., Balderas M., Major A., Runge J., (2018). Postnatal colonization with human “infant-type” Bifidobacterium species alters behavior of adult gnotobiotic mice. PLoS One 13:e0196510. 10.1371/journal.pone.0196510 29763437
64. Mackenzie D. A., Jeffers F., Parker M. L., Vibert-Vallet A., Bongaerts R. J., Roos S., (2010). Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 156(Pt 11), 3368–3378. 10.1099/mic.0.043265-0 20847011
65. Magnusdottir S., Ravcheev D., de Crecy-Lagard V., Thiele I., (2015). Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front. Genet. 6:148. 10.3389/fgene.2015.00148 25941533
66. Markowitz V. M., Chen I. M., Palaniappan K., Chu K., Szeto E., Grechkin Y., (2012). IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res. 40 D115–D122. 10.1093/nar/gkr1044 22194640
67. Maruvada P., Leone V., Kaplan L. M., Chang E. B., (2017). The human microbiome and obesity: moving beyond associations. Cell Host Microbe 22 589–599. 10.1016/j.chom.2017.10.005 29120742
68. Maynard C., Cummins I., Green J., Weinkove D., (2018). A bacterial route for folic acid supplementation. BMC Biol. 16:67. 10.1186/s12915-018-0534-3 29903004
69. McCabe L. R., Irwin R., Schaefer L., Britton R. A., (2013). Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J. Cell Physiol. 228 1793–1798. 10.1002/jcp.24340 23389860
70. McCabe L. R., Parameswaran N., (2018). Advances in probiotic regulation of bone and mineral metabolism. Calcif. Tissue Int. 102 480–488. 10.1007/s00223-018-0403-7 29453726
71. McDougall C. J., Wong R., Scudera P., Lesser M., DeCosse J. J., (1993). Colonic mucosal pH in humans. Dig. Dis. Sci. 38 542–545. 8444087
72. Menon V., Wang X., Greene T., Beck G. J., Kusek J. W., Selhub J., (2005). Homocysteine in chronic kidney disease: effect of low protein diet and repletion with B vitamins. Kidney Int. 67 1539–1546. 10.1111/j.1523-1755.2005.00234.x 15780109
73. Mestas J., Hughes C. C., (2004). Of mice and not men: differences between mouse and human immunology. J. Immunol. 172 2731–2738. 14978070
74. Middendorp S., Schneeberger K., Wiegerinck C. L., Mokry M., Akkerman R. D., van Wijngaarden S., (2014). Adult stem cells in the small intestine are intrinsically programmed with their location-specific function. Stem Cells 32 1083–1091. 10.1002/stem.1655 24496776
75. Million M., Angelakis E., Maraninchi M., Henry M., Giorgi R., Valero R., (2013). Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int. J. Obes. 37 1460–1466. 10.1038/ijo.2013.20 23459324
76. Morowitz M. J., Carlisle E. M., Alverdy J. C., (2011). Contributions of intestinal bacteria to nutrition and metabolism in the critically ill. Surg. Clin. North Am. 91 771–785,viii. 10.1016/j.suc.2011.05.001 21787967
77. Mu Q., Tavella V. J., Luo X. M., (2018). Role of Lactobacillus reuteri in human health and diseases. Front. Microbiol. 9:757. 10.3389/fmicb.2018.00757
78. Nair K. M., Iyengar V., (2009). Iron content, bioavailability & factors affecting iron status of Indians. Indian J. Med. Res. 130 634–645.
79. O’Connor E. M., (2013). The role of gut microbiota in nutritional status. Curr. Opin. Clin. Nutr. Metab. Care 16 509–516. 10.1097/MCO.0b013e3283638eb3 23852088
80. Pitkin R. M., (2007). Folate and neural tube defects. Am. J. Clin. Nutr. 85 285S–288S. 10.1093/ajcn/85.1.285S 17209211
81. Pompei A., Cordisco L., Amaretti A., Zanoni S., Matteuzzi D., Rossi M., (2007a). Folate production by bifidobacteria as a potential probiotic property. Appl. Environ. Microbiol. 73 179–185. 10.1128/AEM.01763-6 17071792
82. Pompei A., Cordisco L., Amaretti A., Zanoni S., Raimondi S., Matteuzzi D., (2007b). Administration of folate-producing bifidobacteria enhances folate status in Wistar rats. J. Nutr. 137 2742–2746. 10.1093/jn/137.12.2742 18029493
83. Qiu A., Jansen M., Sakaris A., Min S. H., Chattopadhyay S., Tsai E., (2006). Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127 917–928. 10.1016/j.cell.2006.09.041 17129779
84. Rajagopalan P. T., Zhang Z., McCourt L., Dwyer M., Benkovic S. J., Hammes G. G., (2002). Interaction of dihydrofolate reductase with methotrexate: ensemble and single-molecule kinetics. Proc. Natl. Acad. Sci. U.S.A. 99 13481–13486. 10.1073/pnas.172501499 12359872
85. Rajan A., Vela L., Zeng X. L., Yu X., Shroyer N., Blutt S. E., (2018). Novel segment- and host-specific patterns of enteroaggregative Escherichia coli adherence to human intestinal enteroids. mBio 9:e02419-17. 10.1128/mBio.02419-7 29463660
86. Rajgopal A., Sierra E. E., Zhao R., Goldman I. D., (2001). Expression of the reduced folate carrier SLC19A1 in IEC-6 cells results in two distinct transport activities. Am. J. Physiol. Cell Physiol. 281 C1579–C1586. 10.1152/ajpcell.2001.281.5.C1579 11600421
87. Robador A., LaRowe D. E., Finkel S. E., Amend J. P., Nealson K. H., (2018). Changes in microbial energy metabolism measured by nanocalorimetry during growth phase transitions. Front. Microbiol. 9:109. 10.3389/fmicb.2018.00109 29449836
88. Rolfe M. D., Rice C. J., Lucchini S., Pin C., Thompson A., Cameron A. D., (2012). Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. J. Bacteriol. 194 686–701. 10.1128/JB.06112-1 22139505
89. Rossi M., Amaretti A., Raimondi S., (2011). Folate production by probiotic bacteria. Nutrients 3 118–134. 10.3390/nu3010118 22254078
90. Roth D., Chiang A. J., Hu W., Gugiu G. B., Morra C. N., Versalovic J., (2019). Two-carbon folate cycle of commensal Lactobacillus reuteri 6475 gives rise to immunomodulatory ethionine, a source for histone ethylation. FASEB J. 33 3536–3548. 10.1096/fj.201801848R 30452879
91. Rowland I., Gibson G., Heinken A., Scott K., Swann J., Thiele I., (2018). Gut microbiota functions: metabolism of nutrients and other food components. Eur. J. Nutr. 1 1–24. 10.1007/s00394-017-1445-8 28393285
92. Said H. M., Mohammed Z. M., (2006). Intestinal absorption of water-soluble vitamins: an update. Curr. Opin. Gastroenterol. 22 140–146. 10.1097/01.mog.0000203870.22706.52 16462170
93. Sato T., Clevers H., (2013). Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340 1190–1194. 10.1126/science.1234852 23744940
94. Sato T., Stange D. E., Ferrante M., Vries R. G., Van Es J. H., Van den Brink S., (2011). Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 141 1762–1772. 10.1053/j.gastro.2011.07.050 21889923
95. Sato T., Vries R. G., Snippert H. J., van de Wetering M., Barker N., Stange D. E., (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459 262–265. 10.1038/nature07935 19329995
96. Saxena K., Blutt S. E., Ettayebi K., Zeng X. L., Broughman J. R., Crawford S. E., (2016). Human intestinal enteroids: a new model to study human rotavirus infection, host restriction, and pathophysiology. J. Virol. 90 43–56. 10.1128/JVI.01930-15 26446608
97. Saxena K., Simon L. M., Zeng X. L., Blutt S. E., Crawford S. E., Sastri N. P., (2017). A paradox of transcriptional and functional innate interferon responses of human intestinal enteroids to enteric virus infection. Proc. Natl. Acad. Sci. U.S.A. 114 E570–E579. 10.1073/pnas.1615422114 28069942
98. Schepper J. D., Collins F. L., Rios-Arce N. D., Raehtz S., Schaefer L., Gardinier J. D., (2019). Probiotic Lactobacillus reuteri prevents postantibiotic bone loss by reducing intestinal dysbiosis and preventing barrier disruption. J. Bone Miner. Res. 34 681–698. 10.1002/jbmr.3635 30690795
99. Scott J. M., (1999). Folate and vitamin B12. Proc. Nutr. Soc. 58 441–448.
100. Shen J., Putt K. S., Visscher D. W., Murphy L., Cohen C., Singhal S., (2015). Assessment of folate receptor-beta expression in human neoplastic tissues. Oncotarget 6 14700–14709. 10.18632/oncotarget.3739 25909292
101. Shimizu J., Kubota T., Takada E., Takai K., Fujiwara N., Arimitsu N., (2018). Propionate-producing bacteria in the intestine may associate with skewed responses of IL10-producing regulatory T cells in patients with relapsing polychondritis. PLoS One 13:e0203657. 10.1371/journal.pone.0203657 30235279
102. Spinler J. K., Sontakke A., Hollister E. B., Venable S. F., Oh P. L., Balderas M. A., (2014). From prediction to function using evolutionary genomics: human-specific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol. Evol. 6 1772–1789. 10.1093/gbe/evu137 24951561
103. Streit W. R., Entcheva P., (2003). Biotin in microbes, the genes involved in its biosynthesis, its biochemical role and perspectives for biotechnological production. Appl. Microbiol. Biotechnol. 61 21–31. 10.1007/s00253-002-1186-2 12658511
104. Tabanelli G., Torriani S., Rossi F., Rizzotti L., Gardini F., (2012). Effect of chemico-physical parameters on the histidine decarboxylase (HdcA) enzymatic activity in Streptococcus thermophilus PRI60. J. Food Sci. 77 M231–M237. 10.1111/j.1750-3841.2012.02628.x 22429258
105. Thomas C. M., Hong T., van Pijkeren J. P., Hemarajata P., Trinh D. V., Hu W., (2012). Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 7:e31951. 10.1371/journal.pone.0031951 22384111
106. Thomas C. M., Saulnier D. M., Spinler J. K., Hemarajata P., Gao C., Jones S. E., (2016). FolC2-mediated folate metabolism contributes to suppression of inflammation by probiotic Lactobacillus reuteri. Microbiologyopen 5 802–818. 10.1002/mbo3.371 27353144
107. VanDussen K. L., Marinshaw J. M., Shaikh N., Miyoshi H., Moon C., Tarr P. I., (2015). Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut 64 911–920. 10.1136/gutjnl-2013-306651 25007816
108. Visentin M., Diop-Bove N., Zhao R., Goldman I. D., (2014). The intestinal absorption of folates. Annu. Rev. Physiol. 76 251–274. 10.1146/annurev-physiol-020911-153251 24512081
109. Vollset S. E., Clarke R., Lewington S., Ebbing M., Halsey J., Lonn E., (2013). Effects of folic acid supplementation on overall and site-specific cancer incidence during the randomised trials: meta-analyses of data on 50,000 individuals. Lancet 381 1029–1036. 10.1016/S0140-6736(12)62001-7 23352552
110. Walter J., Chagnaud P., Tannock G. W., Loach D. M., Dal Bello F., Jenkinson H. F., (2005). A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl. Environ. Microbiol. 71 979–986. 10.1128/AEM.71.2.979-986.2005 15691956
111. Wang X., Cabrera R. M., Li Y., Miller D. S., Finnell R. H., (2013). Functional regulation of P-glycoprotein at the blood-brain barrier in proton-coupled folate transporter (PCFT) mutant mice. FASEB J. 27 1167–1175. 10.1096/fj.12-218495 23212123
112. Wibowo A. S., Singh M., Reeder K. M., Carter J. J., Kovach A. R., Meng W., (2013). Structures of human folate receptors reveal biological trafficking states and diversity in folate and antifolate recognition. Proc. Natl. Acad. Sci. U.S.A. 110 15180–15188. 10.1073/pnas.1308827110 23934049
113. Yin Y., Bijvelds M., Dang W., Xu L., van der Eijk A. A., Knipping K., (2015). Modeling rotavirus infection and antiviral therapy using primary intestinal organoids. Antiviral Res. 123 120–131. 10.1016/j.antiviral.2015.09.010 26408355
114. Yin Y., Zhou D., (2018). Organoid and enteroid modeling of Salmonella infection. Front. Cell Infect. Microbiol. 8:102. 10.3389/fcimb.2018.00102 29670862
115. Zachos N. C., Kovbasnjuk O., Foulke-Abel J., In J., Blutt S. E., de Jonge H. R., (2016). Human enteroids/colonoids and intestinal organoids functionally recapitulate normal intestinal physiology and pathophysiology. J. Biol. Chem. 291 3759–3766. 10.1074/jbc.R114.635995 26677228
116. Zhao R., Goldman I. D., (2007). The molecular identity and characterization of a proton-coupled folate transporter–PCFT; biological ramifications and impact on the activity of pemetrexed. Cancer Metastasis Rev. 26 129–139. 10.1007/s10555-007-9047-1 17340171
117. Zhao R., Goldman I. D., (2013). Folate and thiamine transporters mediated by facilitative carriers (SLC19A1-3 and SLC46A1) and folate receptors. Mol. Aspects Med. 34 373–385. 10.1016/j.mam.2012.07.006 23506878
118. Zou W. Y., Blutt S. E., Crawford S. E., Ettayebi K., Zeng X. L., Saxena K., (2017). Human intestinal enteroids: new models to study gastrointestinal virus infections. Methods Mol. Biol. 1576 229–247. 10.1007/7651_2017_1 28361480