Evaluation of growth, metabolism and production of potentially bioactive components during fermentation of barley with Lactobacillus reuteri

Food Microbiology

Volumn 57, Issue , 2016, Pages 159-171

  Pallin, Anton ^a   Agback, Peter ^a   Jonsson, Hans ^a   Roos, Stefan ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

1H NMR; Barley; Bioactive compounds; Fermented cereals; Lactobacillus reuteri

Indexed keywords

1,3-PROPANEDIOL; 4 AMINOBUTYRIC ACID; HISTAMINE; PROPANEDIOL DERIVATIVE;

CHEMISTRY; FERMENTATION; FLOUR; FOOD CONTROL; GROWTH, DEVELOPMENT AND AGING; HORDEUM; LACTOBACILLUS REUTERI; METABOLISM; MICROBIOLOGY;

FERMENTATION; FLOUR; FOOD MICROBIOLOGY; GAMMA-AMINOBUTYRIC ACID; HISTAMINE; HORDEUM; LACTOBACILLUS REUTERI; PROPYLENE GLYCOLS;

EID: 84960113299     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2016.02.011     Document Type: Article

References (61)

1. Arena M.P., Caggianiello G., Fiocco D., Russo P., Torelli M., Spano G., Capozzi V. Barley β-glucans-containing food enhances probiotic performances of beneficial bacteria. Int. J. Mol. Sci 2014, 15(2):3025-3039.
2. Benavent-Gil Y., Berbegal C., Lucio O., Pardo I., Ferrer S. A new fear in wine: isolation of Staphylococcus epidermidis histamine producer. Food Control 2016, 62:142-149.
3. Biesalski H.-K., Dragsted L.O., Elmadfa I., Grossklaus R., Müller M., Schrenk D., Walter P., Weber P. Bioactive compounds: definition and assessment of activity. Nutrition 2009, 25(11-12):1202-1205.
4. Capozzi V., Russo P., Dueñas M.T., López P., Spano G. Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products. Appl. Microbiol. Biotechnol. 2012, 96(6):1383-1394.
5. Charalampopoulos D., Pandiella S., Webb C. Growth studies of potentially probiotic lactic acid bacteria in cereal-based substrates. J. Appl. Microbiol. 2002, 92(5):851-859.
6. Charalampopoulos D., Vázquez J.A., Pandiella S.S. Modelling and validation of Lactobacillus plantarum fermentations in cereal-based media with different sugar concentrations and buffering capacities. Biochem. Eng. J. 2009, 44(2):96-105.
7. Chung T., Axelsson L., Lindgren S., Dobrogosz W. In vitro studies on reuterin synthesis by Lactobacillus reuteri. Microb. Ecol. Health Dis. 1989, 2(2):137-144.
8. Contrepois K., Jiang L., Snyder M. Optimized analytical procedures for the untargeted metabolomic profiling of human urine and plasma by combining Hydrophilic Interaction (HILIC) and Reverse-Phase Liquid Chromatography (RPLC)-Mass Spectrometry. Mol. Cell. Proteom. 2015, 14(6):1684-1695.
9. Dal Bello F., Walter J., Roos S., Jonsson H., Hertel C. Inducible gene expression in Lactobacillus reuteri LTH5531 during type II sourdough fermentation. Appl. Environ. Microbiol. 2005, 71(10):5873-5878.
10. De Vuyst L., Van Kerrebroeck S., Harth H., Huys G., Daniel H.-M., Weckx S. Microbial ecology of sourdough fermentations: diverse or uniform?. Food Microbiol. 2014, 37:11-29.
11. Edwards U., Rogall T., Blöcker H., Emde M., Böttger E.C. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 1989, 17(19):7843-7853.
12. Emara M.H., Mohamed S.Y., Abdel-Aziz H.R. Lactobacillus reuteri in management of Helicobacter pylori infection in dyspeptic patients: a double-blind placebo-controlled randomized clinical trial. Ther. Adv. Gastroenterol. 2014, 7(1):4-13.
13. FAO Most Produced Commodities in Sweden 2010-2013 2014, [29.01.15]. http://faostat3.fao.org.
14. Gao C., Major A., Rendon D., Lugo M., Jackson V., Shi Z., Mori-Akiyama Y., Versalovic J. Histamine H2 receptor-mediated suppression of intestinal inflammation by probiotic Lactobacillus reuteri. mBio 2015, 6(6):e01358-15.
15. Gänzle M.G., Vogel R.F. Contribution of reuteri cyclin production to the stable persistence of Lactobacillus reuteri in an industrial sourdough fermentation. Int. J. Food Microbiol. 2003, 80(1):31-45.
16. Gänzle M.G., Zhang C., Monang B.-S., Lee V., Schwab C. Novel metabolites from cereal-associated lactobacilli - Novel functionalities for cereal products?. Food Microbiol. 2009, 26(7):712-719.
17. Giger-Reverdin S., Duvaux-Ponter C., Sauvant D., Martin O., Nunes do Prado I., Müller R. Intrinsic buffering capacity of feedstuffs. Animal Feed Sci. Technol. 2002, 96(1-2):83-102.
18. Gomes A.M.P., Malcata F.X. Bifidobacterium spp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Trends Food Sci. Technol. 1999, 10(4-5):139-157.
19. Hammes W.P., Hertel C. The genera Lactobacillus and carnobacterium. The Prokaryotes 2006, 320-403. Springer.
20. Hara H., Haga S., Aoyama Y., Kiriyama S. Short-chain fatty acids suppress cholesterol synthesis in rat liver and intestine. J. Nutr. 1999, 129(5):942-948.
21. Hemarajata P., Gao C., Pflughoeft K., Thomas C., Saulnier D., Spinler J., Versalovic J. Lactobacillus reuteri-specific immunoregulatory gene rsiR modulates histamine production and immunomodulation by Lactobacillus reuteri. J. Bacteriol 2013, 195(24):5567-5576.
22. Hidalgo-Morales M., Robles-Olvera V., García H.S. Lactobacillus reuteri β-galactosidase activity and low milk acidification ability. Can. J. Microbiol. 2005, 51(3):261-267.
23. Hii S.L., Tan J.S., Ling T.C., Ariff A.B. Pullulanase: role in starch hydrolysis and potential industrial applications. Enzyme Res. 2012, 2012.
24. Hoben H., Somasegaran P. Comparison of the pour, spread, and drop plate methods for enumeration of Rhizobium spp. in inoculants made from presterilized peat. Appl. Environ. Microbiol. 1982, 44(5):1246-1247.
25. Hole A.S., Rud I., Grimmer S., Sigl S., Narvhus J., Sahlstrøm S. Improved bioavailability of dietary phenolic acids in whole grain barley and oat groat following fermentation with probiotic Lactobacillus acidophilus, Lactobacillus johnsonii, and Lactobacillus reuteri. J. Agric. Food Chem. 2012, 60(25):6369-6375.
26. Hüfner E., Britton R.A., Roos S., Jonsson H., Hertel C. Global transcriptional response of Lactobacillus reuteri to the sourdough environment. Syst. Appl. Microbiol. 2008, 31(5):323-338.
27. Johansson M.L., Molin G., Pettersson B., Uhlen M., Ahrne S. Characterization and species recognition of Lactobacillus plantarum strains by restriction fragment length polymorphism (RFLP) of the 16S rRNA gene. J. Appl. Bacteriol. 1995, 79(5):536-541.
28. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P., Drummond A. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28(12):1647-1649.
29. Keenan J.M., Goulson M., Shamliyan T., Knutson N., Kolberg L., Curry L. The effects of concentrated barley β-glucan on blood lipids in a population of hypercholesterolaemic men and women. Br. J. Nutr. 2007, 97(06):1162-1168.
30. Letunic I., Bork P. Interactive Tree of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007, 23(1):127-128.
31. Makhoul S., Romano A., Capozzi V., Spano G., Aprea E., Cappellin L., Benozzi E., Scampicchio M., Märk T.D., Gasperi F. Volatile compound production during the Bread-Making Process: effect of flour, yeast and their interaction. Food Bioprocess Technol 2015, 8(9):1925-1937.
32. McDonald L., Fleming H., Hassan H. Acid tolerance of Leuconostoc mesenteroides and Lactobacillus plantarum. Appl. Environ. Microbiol. 1990, 56(7):2120-2124.
33. Meroth C.B., Walter J., Hertel C., Brandt M.J., Hammes W.P. Monitoring the bacterial population dynamics in sourdough fermentation processes by using pcr-denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 2003, 69(1):475-482.
34. Müller M.R., Wolfrum G., Stolz P., Ehrmann M.A., Vogel R.F. Monitoring the growth of Lactobacillus species during a rye flour fermentation. Food Microbiol. 2001, 18(2):217-227.
35. Muyzer G., De Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59(3):695-700.
36. Oh P.L., Benson A.K., Peterson D.A., Patil P.B., Moriyama E.N., Roos S., Walter J. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J. 2009, 4(3):377-387.
37. Rai K.P., Pradhan H.R., Sharma B.K., Rijal S.K. Histamine in foods: its safety and human health implications. J. Food Sci. Technol. Nepal 2014, 8:1-11.
38. Romani Vestman N., Hasslöf P., Keller M.K., Granström E., Roos S., Twetman S., Stecksén-Blicks C. Lactobacillus reuteri influences regrowth of Mutans streptococci after Full-Mouth Disinfection: a double-blind, randomised controlled trial. Caries Res 2013, 47(4):338-345.
39. Rosander A., Connolly E., Roos S. Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl. Environ. Microbiol. 2008, 74(19):6032-6040.
40. Russo P., Capozzi V., Arena M.P., Spadaccino G., Dueñas M.T., López P., Fiocco D., Spano G. Riboflavin-overproducing strains of Lactobacillus fermentum for riboflavin-enriched bread. Appl. Microbiol. Biotechnol. 2014, 98(8):3691-3700.
41. Sanders J.W., Venema G., Kok J. Environmental stress responses in Lactococcus lactis. FEMS Microbiol. Rev. 1999, 23(4):483-501.
42. Saulnier D.M., Santos F., Roos S., Mistretta T.-A., Spinler J.K., Molenaar D., Teusink B., Versalovic J. Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. PloS one 2011, 6(4):e18783.
43. Savino F., Cordisco L., Tarasco V., Palumeri E., Calabrese R., Oggero R., Roos S., Matteuzzi D. Lactobacillus reuteri DSM 17938 in infantile colic: a randomized, double-blind, placebo-controlled trial. Pediatrics 2010, 126(3):e526-e533.
44. Shen R.-L., Dang X.-Y., Dong J.-L., Hu X.-Z. Effects of oat β-glucan and barley β-glucan on fecal characteristics, intestinal microflora, and intestinal bacterial metabolites in rats. J. Agric. Food Chem. 2012, 60(45):11301-11308.
45. Shimizu C., Kihara M., Aoe S., Araki S., Ito K., Hayashi K., Watari J., Sakata Y., Ikegami S. Effect of high β-glucan barley on serum cholesterol concentrations and visceral fat area in japanese men-a randomized, double-blinded, placebo-controlled trial. Plant Foods Hum. Nutr. 2008, 63(1):21-25.
46. Silvestro D., Michalak I. raxmlGUI: a graphical front-end for RAxML. Org. Divers. Evol. 2012, 12(4):335-337.
47. Song Y.-L., Kato N., Liu C.-X., Matsumiya Y., Kato H., Watanabe K. Rapid identification of 11 human intestinal Lactobacillus species by multiplex PCR assays using group-and species-specific primers derived from the 16S-23S rRNA intergenic spacer region and its flanking 23S rRNA. FEMS Microbiol. Lett. 2000, 187(2):167-173.
48. Spinler J.K., Taweechotipatr M., Rognerud C.L., Ou C.N., Tumwasorn S., Versalovic J. Human-derived probiotic Lactobacillus reuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 2008, 14(3):166-171.
49. Stolz P., Vogel R.F., Hammes W.P. Utilization of electron acceptors by lactobacilli isolated from sourdough. Z. für Lebensm. Forsch. 1995, 201(4):402-410.
50. Stromeck A., Hu Y., Chen L., Gänzle M.G. Proteolysis and bioconversion of cereal proteins to glutamate and γ-aminobutyrate (GABA) in rye malt sourdoughs. J. Agric. Food Chem. 2011, 59(4):1392-1399.
51. Su M.S.-W., Oh P.L., Walter J., Gänzle M.G. Intestinal origin of sourdough Lactobacillus reuteri isolates as revealed by phylogenetic, genetic, and physiological analysis. Appl. Environ. Microbiol. 2012, 78(18):6777-6780.
52. Tapingkae W., Tanasupawat S., Parkin K.L., Benjakul S., Visessanguan W. Degradation of histamine by extremely halophilic archaea isolated from high salt-fermented fishery products. Enzyme Microb. Technol 2010, 46(2):92-99.
53. Tedelind S., Westberg F., Kjerrulf M., Vidal A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World J. Gastroenterol. 2007, 13(20):2826-2832.
54. Thomas C.M., Hong T., van Pijkeren J.P., Hemarajata P., Trinh D.V., Hu W., Britton R.A., Kalkum M., Versalovic J. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS One 2012, 7(2):e31951.
55. Versalovic J., Schneider M., De Bruijn F.J., Lupski J.R. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. 1994, 5(1):25-40.
56. Vorkas P.A., Isaac G., Anwar M.A., Davies A.H., Want E.J., Nicholson J.K., Holmes E. Untargeted UPLC-MS profiling pipeline to expand tissue metabolome coverage: application to cardiovascular disease. Anal. Chem. 2015, 87(8):4184-4193.
57. Walter J., Britton R.A., Roos S. Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc. Natl. Acad. Sci. 2011, 108(Suppl. 1):4645-4652.
58. Wehrle K., Crowe N., van Boeijen I., Arendt E.K. Screening methods for the proteolytic breakdown of gluten by lactic acid bacteria and enzyme preparations. Eur. Food Res. Technol. 1999, 209(6):428-433.
59. Weizman Z., Asli G., Alsheikh A. Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics 2005, 115(1):5-9.
60. Wong J.M., de Souza R., Kendall C.W., Emam A., Jenkins D.J. Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol. 2006, 40(3):235-243.
61. Zelante T., Iannitti R.G., Cunha C., De Luca A., Giovannini G., Pieraccini G., Zecchi R., D'Angelo C., Massi-Benedetti C., Fallarino F. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013, 39(2):372-385.