Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides

Applied Microbiology and Biotechnology

Volumn 100, Issue 3, 2016, Pages 1121-1135

  Zannini, Emanuele ^a   Waters, Deborah M ^a   Coffey, Aidan ^b   Arendt, Elke K ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b Munster Technological University   (Ireland)

Author keywords

EPS industry applications; Exopolysaccharides; Food fermentation; Lactic acid bacteria

Indexed keywords

FOOD PRODUCTS; INDUSTRIAL RESEARCH; LACTIC ACID; METABOLITES; POLYSACCHARIDES;

ACADEMIC RESEARCH; CHEMICAL COMPOSITIONS; CONCRETE APPLICATIONS; EXOPOLYSACCHARIDES; FOOD FERMENTATION; INDUSTRY APPLICATIONS; LACTIC ACID BACTERIA; STRUCTURAL DIVERSITY;

BACTERIA;

ALTERNAN; BACTERIAL POLYSACCHARIDE; BETA GLUCAN; DEXTRAN; EXOPOLYSACCHARIDE; FRUCTAN; INULIN; LEVAN; MUTAN; REUTERAN; UNCLASSIFIED DRUG;

BACTERIUM; BIOTECHNOLOGY; EXOPOLYMER; FEASIBILITY STUDY; FERMENTATION; FOOD INDUSTRY; FOOD PRODUCTION; INDUSTRIAL PRACTICE; MICROBIOLOGY; ORGANIC ACID; POLYSACCHARIDE;

BACTERIAL STRAIN; CARBON SOURCE; CHEMICAL COMPOSITION; CONFORMATIONAL TRANSITION; ENZYME CONFORMATION; FEASIBILITY STUDY; FERMENTATION; FOOD INDUSTRY; HUMAN; HYDROCOLLOID; LACTIC ACID BACTERIUM; LACTOBACILLUS REUTERI; LEUCONOSTOC MESENTEROIDES; MOLECULAR WEIGHT; NONHUMAN; PH; REVIEW; SPECIES; STREPTOCOCCUS MUTANS; VISCOSITY; VOLATILIZATION; BIOSYNTHESIS; CHEMISTRY; FOOD CONTROL; GENETICS; LACTOBACILLUS; METABOLISM; PROCEDURES; TRENDS;

BACTERIA (MICROORGANISMS);

FERMENTATION; FOOD MICROBIOLOGY; LACTOBACILLUS; POLYSACCHARIDES, BACTERIAL;

EID: 84955197436     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-7172-2     Document Type: Review

References (177)

1. Aebischer J, D’amico N, De Maleprade D, Eyer K, Lesens C, Neeser JR, Reniero R, Schmid D (2001) Products containing a dextran composition obtained from culturing Leuconostoc mesenteroides ssp. cremoris. Patent N. Us6004800
2. Anwar MA, Kralj S, Van Der Maarel MJEC, Dijkhuizen L (2008) The probiotic Lactobacillus johnsonii NCC 533 produces high-molecular-mass inulin from sucrose by using an inulosucrase enzyme. Appl Environ Microb 74:3426–3433. doi:10.1128/Aem.00377-08
3. Anwar MA, Kralj S, Piqué AV, Leemhuis H, Van Der Maarel MJEC, Dijkhuizen L (2010) Inulin and levan synthesis by probiotic Lactobacillus gasseri strains: characterization of three novel fructansucrase enzymes and their fructan products. Microbiology 156:1264–1274. doi:10.1099/Mic.0.036616-0
4. Arendt EK, Lam R, Dal Bello F (2007) Impact of sourdough on the texture of bread. Food Microbiol 24:165–174. doi:10.1016/J.Fm.2006.07.011
5. Argüello-Morales MA, Remaud-Simeon M, Pizzut S, Sarçabal P, Willemot R-M, Monsan P (2000) Sequence analysis of the gene encoding alternansucrase, a sucrose glucosyltransferase from Leuconostoc mesenteroides NRRL B-1355 182:81–85. doi:10.1111/J.1574-6968.2000.Tb08878.X
6. Badel S, Bernardi T, Michaud P (2011) New perspectives for Lactobacilli exopolysaccharides. Biotechnol Adv 29:54–66. doi:10.1016/J.Biotechadv.2010.08.011
7. Bhavani AL, Nisha J (2010) Dextran—the polysaccharide with versatile uses. Int J Pharma Bio Sci 1:569
8. Bounaix M-S, Gabriel V, Robert H, Morel S, Remaud-Siméon M, Gabriel B, Fontagné-Faucher C (2010) Characterization of glucan-producing Leuconostoc strains isolated from sourdough. Int J Food Microbiol 144:1–9. doi:10.1016/J.Ijfoodmicro.2010.05.026
9. Broadbent JR, Mcmahon DJ, Oberg CJ, Welker DL (2001) Use of exopolysaccharide-producing cultures to improve the functionality of low fat cheese. Int Dairy J 11:433–439. doi:10.1016/S0958-6946(01)00084-X
10. Buchholz K, Seibel J (2008) Industrial carbohydrate biotransformations. Carbohyd Res 343:1966–1979. doi:10.1016/J.Carres.2008.02.007
11. Byrne D (2001) Commission Decision of 30 January 2001 on authorising the placing on the market of a dextran preparation produce by Leuconostoc mesenteroidesas a novel food ingredients in bakery products under Regulation (EC) No. 258/97 of the European Parliament and of the Concil Official Journal European Commission L44, Bruxells
12. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238. doi:10.1093/Nar/Gkn663
13. Cardarelli HR, Aragon-Alegro LC, Alegro JHA, De Castro IA, Saad SMI (2008) Effect of inulin and Lactobacillus paracasei on sensory and instrumental texture properties of functional chocolate mousse. J Sci Food Agric 88:1318–1324
14. Cerning J (1990) Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiol Lett 87:113–130. doi:10.1111/J.1574-6968.1990.Tb04883.X
15. Cerning J (1995) Production of exopolysaccharides by lactic acid bacteria and dairy propionibacteria. Lait 75:463–472
16. Chapot-Chartier MP, Monnet V, De Vuyst L (2011) Cell walls and exopolysaccharides of lactic acid bacteria. In: Ledeboer A, Hugenholtz J, Kok J, Konings W, Wouters J (eds) Thirty Years Of Research On Lactic Acid Bacteria. Media Labs, Rotterdam, The Netherlands, pp 113–132
17. Colby SM, Russell RRB (1997) Sugar metabolism by mutans Streptococci. J Appl Microbiol 83:80s–88s. doi:10.1046/J.1365-2672.83.S1.9.X
18. Côté GL (2002) Alternan. In: Vandamme E, Debaets S, Steinbuchel A (eds) Biopolymers. Wiley-Vch, Weinheim, Germany, pp 323–350
19. Côté GL (2009) Acceptor products of alternansucrase with gentiobiose. Production of novel oligosaccharides for food and feed and elimination of bitterness. Carbohyd Res 344:187–190. doi:10.1016/J.Carres.2008.10.017
20. Côté GL, Robyt JF (1982a) Isolation and partial characterization of an extracellular glucansucrase from Leuconostoc mesenteroides NRRL B-1355 that synthesizes an alternating (1-6), (1-3)-alpha-D-glucan. Carbohyd Res 101:57–74. doi:10.1016/S0008-6215(00)80795-8
21. Côté GL, Robyt JF (1982b) Isolation and partial characterization of an extracellular glucansucrase from Leuconostoc mesenteroides NRRL B-1355 that synthesizes an alternating (1→6), (1→3)-Α-D-glucan. Carbohyd Res 101:57–74
22. Côté GL, Skory C (2012) Cloning, expression, and characterization of an insoluble glucan-producing glucansucrase from Leuconostoc mesenteroides NRRL B-1118. Appl Microbiol Biot 93:2387–2394. doi:10.1007/S00253-011-3562-2
23. Cote GL, Leathers TD, Ahlgren JA, Wyckoff HA, Hayman GT, Biely P (1997) Chapter 8. Alternan and highly branched limit dextrans: low-viscosity polysaccharides as potential new food ingredients. In: Okai H, Mills O, Spanier AM, Tamura M (eds) Chemistry of Novel Foods. ACS Symposium Series, pp 95–109
24. Côté GL, Skory C, Unser S, Rich J (2013) The production of glucans via glucansucrases from Lactobacillus satsumensis isolated from a fermented beverage starter culture. Appl Microbiol Biot 97:7265–7273. doi:10.1007/S00253-012-4606-Y
25. De Vuyst L, Degeest B (1999) Heteropolysaccharides from lactic acid bacteria. Fems Microbiol Rev 23:153–177. doi:10.1016/S0168-6445(98)00042-4
26. De Vuyst L, De Vin F, Vaningelgem F, Degeest B (2001) Recent developments in the biosynthesis and applications of heteropolysaccharides from lactic acid bacteria. Int Dairy J 11:687–707. doi:10.1016/S0958-6946(01)00114-5
27. Degeest B, Vaningelgem F, De Vuyst L (2001) Microbial physiology, fermentation kinetics, and process engineering of heteropolysaccharide production by lactic acid bacteria. Int Dairy J 11:747–757. doi:10.1016/S0958-6946(01)00118-2
28. Degeest B, Mozzi F, De Vuyst L (2002) Effect of medium composition and temperature and ph changes on exopolysaccharide yields and stability during Streptococcus thermophilus LY03 fermentations. Int J Food Microbiol 79:161–174. doi:10.1016/S0168-1605(02)00116-2
29. Dertli E, Mayer MJ, Narbad A (2015) Impact of the exopolysaccharide layer on biofilms, adhesion and resistance to stress in Lactobacillus johnsonii FI9785. BMC Microbiol 15:8. doi:10.1186/S12866-015-0347-2
30. Dierksen KP, Sandine WE, Trempy JE (1997) Expression of ropy and mucoid phenotypes in Lactococcus lactis. J Dairy Sci 80:1528–1536. doi:10.3168/Jds.S0022-0302(97)76082-X
31. Duboc P, Mollet B (2001) Applications of exopolysaccharides in the dairy industry. Int Dairy J 11:759–768. doi:10.1016/S0958-6946(01)00119-4
32. Duenas-Chasco HT, Rodriguez-Carvajal MA, Mateo PT, Franco-Rodriguez G, Espartero JL, Irastorza-Iribas A, Gil-Serrano AM (1997) Structural analysis of the exopolysaccharide produced by Pediococcus damnosus 2.6. Carbohyd Res 303:453–458
33. Duenas-Chasco MT, Rodriguez-Carvajal MA, Tejero-Mateo P, Espartero JL, Irastorza-Iribas A, Gil-Serrano AM (1998) Structural analysis of the exopolysaccharides produced by Lactobacillus spp. G-77. Carbohyd Res 307:125–133. doi:10.1016/S0008-6215(98)00034-2
34. Ernst MK, Chatterton NJ, Harrison PA, Matitschka G (1998) Characterization of fructan oligomers from species of the genus Allium L. J Plant Physiol 153:53–60
35. FDA (2013) Code of federal regulations title 21, Sec. 186.1275 Dextrans. http://www.Accessdata.Fda.Gov/Scripts/Cdrh/Cfdocs/Cfcfr/Cfrsearch.Cfm?Fr=186.1275
36. Figures WR, Edwards JR (1981) D-Glucosyltransferase of Streptococcus mutans: isolation of two forms of the enzyme that bind to insoluble dextran. Carbohyd Res 88:107–117. doi:10.1016/S0008-6215(00)84605-4
37. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. doi:10.1038/Nrmicro2415
38. Fox PF, Uniacke-Lowe T, Mcsweeney PLH, O’mahony JA (2015) Chemistry and biochemistry of fermented milk products. In: Dairy chemistry and biochemistry. Springer Int Publ. Pp 547–567. doi:10.1007/978-3-319-14892-2_13
39. Franck A (2002) Technological functionality of inulin and oligofructose. Br J Nutr 87(Suppl 2):S287–291. doi:10.1079/Bjnbjn/2002550
40. Freitas F, Alves VD, Reis MAM (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends In Biotechnology 29:388–398. doi:10.1016/J.Tibtech.2011.03.008
41. Galle S, Schwab C, Arendt E, Ganzle M (2010) Exopolysaccharide-forming Weissella strains as starter cultures for sorghum and wheat sourdoughs. J Agr Food Chem 58:5834–5841. doi:10.1021/Jf1002683
42. Gibson GR, Beatty ER, Wang X, Cummings JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin gastroenterology 108:975–982. doi 10.1016/0016-5085(95)90192-2
43. Giffard PM, Simpson CL, Milward CP, Jacques NA (1991) Molecular characterization of a cluster of at least 2 glucosyltransferase genes in Streptococcus salivarius ATCC-25975. J Gen Microbiol 137:2577–2593
44. Giffard PM, Allen DM, Milward CP, Simpson CL, Jacques NA (1993) Sequence of the Gtfk gene of Streptococcus Salivarius ATCC 25975 and evolution of the Gtf genes of oral Streptococci. J Gen Microbiol 139:1511–1522
45. Gindreau E, Walling E, Lonvaud-Funel A (2001) Direct polymerase chain reaction detection of ropy Pediococcus damnosus strains in wine. J Appl Microbiol 90:535–542. doi:10.1046/J.1365-2672.2001.01277.X
46. Goulas AK, Fisher DA, Grimble GK, Grandison AS, Rastall RA (2004) Synthesis of isomaltooligosaccharides and oligodextrans by the combined use of dextransucrase and dextranase enzyme. Microb Tech 35:327–338. doi:10.1016/J.Enzmictec.2004.05.008
47. Grobben GJ, Boels IC, Sikkema J, Smith MR, De Bont JAM (2000) Influence of ions on growth and production of exopolysaccharides by Lactobacillus delbrueckii subsp bulgaricus NCFB 2772. J Dairy Res 67:131–135. doi:10.1017/S002202999900391x
48. Gruter M, Leeflang BR, Kuiper J, Kamerling JP, Vliegenthart JFG (1992) Structure of the exopolysaccharide produced by Lactococcus lactis sub cremoris H414 grown in a defined medium or skimmed-milk. Carbohyd Res 231:273–291. doi:10.1016/0008-6215(92)84025-N
49. Guggisberg D, Cuthbert-Steven J, Piccinali P, Bütikofer U, Eberhard P (2009) Rheological, microstructural and sensory characterization of low-fat and whole milk set yoghurt as influenced by inulin addition. Int Dairy J 19:107–115
50. Guven M, Yasar K, Karaca OB, Hayaloglu AA (2005) The effect of inulin as a fat replacer on the quality of set-type low-fat yogurt manufacture. Int J Dairy Technol 58:180–184
51. Hamada S, Slade HD (1980) Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol Rev 44:331–384
52. Hammes WP, Stolz P, Gänzle M (1996) Metabolism of lactobacilli in traditional sourdoughs. Adv Food Sci 18:176–184
53. Han YW (1990) Microbial Levan. In: Saul LN, Allen IL (Eds) Advances in applied microbiology, Vol Volume 35. Academic Press, Pp 171–194. doi:10.1016/S0065-2164(08)70244-2
54. Han YW, Clarke MA (1990) Production and characterization of microbial levan. J Agr Food Chem 38:393–396. doi:10.1021/Jf00092a011
55. He Z, Liang J, Tang Z, Ma R, Peng H, Huang Z (2015) Role of luxS gene in initial biofilm formation by Streptococcus mutans. J Mol Microbiol Biotechnol 25:60–68
56. Hehre EJ, Sugg JY (1942) Serologically reactive polysaccharides produced through the action of bacterial enzymes: I. Dextran of Leuconostoc mesenteroides from sucrose. J Exp Med 75:339–353
57. Hennelly PJ, Dunne PG, O’sullivan M, O’riordan ED (2006) Textural, rheological and microstructural properties of imitation cheese containing inulin. J Food Eng 75:388–395
58. Hestrin S, Avineri-Shapiro S, Aschner M (1943) The enzymic production of levan. Biochem J 37:450–456
59. Hosono A, Lee JW, Ametani A, Natsume M, Hirayama M, Adachi T, Kaminogawa S (1997) Characterization of a water-soluble polysaccharide fraction with immunopotentiating activity from Bifidobacterium adolescentis M101-4. Biosci Biotech Bioch 61:312–316
60. Imeson A (2010) Food stabilisers, thickening and gelling agents. Wiley-Blackwell, Oxford
61. Jang KH, Song KB, Kim CH, Chung BH, Kang SA, Chun UH (2001) Biotechnol Lett 23:39–44
62. Jeanes A, Haynes WC, Wilham CA, Rankin JC, Melvin EH, Austin MJ, Cluskey JE, Fisher BE, Tsuchiya HM, Rist CE (1954) Characterization and classification of dextrans from ninety-six strains of bacteria 1b. J Am Chem Soc 76:5041–5052. doi:10.1021/Ja01649a011
63. Jolly L, Vincent SF, Duboc P, Neeser J-R (2002) Exploiting exopolysaccharides from lactic acid bacteria. Antonie Van Leeuwenhoek 82:367–374. doi:10.1023/A:1020668523541
64. Kang TH, Jung SJ, Kang S, Jang KH, Jang EK, Kim S, Kim IH, Kim CH, Rhee SK, Chun UH (2002) Preparation of levan oligosaccharides by acid hydrolysis and its application in growth of lactic acid-producing bacteria. Korean J Biotechnol Bioeng 17:137–141
65. Kasapis S, Morris E, Gross M, Rudolph K (1994) Solution properties of levan polysaccharide from Pseudomonas syringae pv. phaseolicola, and its possible primary role as a blocker of recognition during pathogenesis. Carbohyd Polym 23:55–64. doi:10.1016/0144-8617(94)90090-6
66. Kebler LF (1921) California bees. J Am Pharm Assoc 10:939–943
67. Kim DS, Fogler HS (1999) The effects of exopolymers on cell morphology and culturability of Leuconostoc mesenteroides during starvation. Appl Microbiol Biot 52:839–844
68. Kim D, Robyt JF (1994) Production and selection of mutants of Leuconostoc mesenteroides constitutive for glucansucrases. Enzyme Microb Tech 16:659–664. doi:10.1016/0141-0229(94)90086-8
69. Kim CH, Song KB, Rhee SK (1998) Viscosity of levan produced by levansucrase from Zymomonas mobilis. Food Eng Prog 2:217–222
70. Kim D, Robyt JF, Lee S-Y, Lee J-H, Kim Y-M (2003) Dextran molecular size and degree of branching as a function of sucrose concentration, ph, and temperature of reaction of Leuconostoc mesenteroides B-512FMCM dextransucrase. Carbohyd Res 338:1183–1189. doi:10.1016/S0008-6215(03)00148-4
71. King M, Speert DP (2002) Use of dextran and other polysaccharides to improve mucus clearance. Patentn. Wo1999001141 A1
72. Kip P, Meyer D, Jellema R (2006) Inulins improve sensoric and textural properties of low-fat yoghurts. Int Dairy J 16:1098–1103
73. Kitazawa H, Toba T, Itoh T, Kumano N, Adachi S, Yamaguchi T (1991) Antitumoral activity of slime-forming, encapsulated Lctococcus lactis subsp. cremoris isolated from Scandinavian Ropy Sour Milk, “viili”. Nihon Chikusan Gakkaiho 62:277–283. doi:10.2508/Chikusan.62.277
74. Knoshaug EP, Ahlgren JA, Trempy JE (2007) Exopolysaccharide expression in Lactococcus lactis subsp. cremoris Ropy352: evidence for novel gene organization. Appl Environ Microb 73:897–905. doi:10.1128/Aem.01945-06
75. Koca N, Metin M (2004) Textural, melting and sensory properties of low-fat fresh kashar cheeses produced by using fat replacers. Int Dairy J 14:365–373
76. Korakli M, Vogel RF (2006) Structure/function relationship of homopolysaccharide producing glycansucrases and therapeutic potential of their synthesised glycans. Appl Microbiol Biot 71:790–803. doi:10.1007/S00253-006-0469
77. Korakli M, Schwarz E, Wolf G, Hammes WP (2000) Production of mannitol by Lactobacillus sanfranciscensis. Adv Food Sci 22:1–4
78. Korakli M, Pavlovic M, Gänzle MG, Vogel RF (2003) Exopolysaccharide and kestose production by Lactobacillus sanfranciscensis LTH2590. Appl Environ Microb 69:2073–2079. doi:10.1128/Aem.69.4.2073-2079.2003
79. Kralj S, Van Geel-Schutten GH, Rahaoui H, Leer RJ, Faber EJ, Van Der Maarel MJEC, Dijkhuizen L (2002) Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with alpha-(1->4) and alpha-(1->6) glucosidic bonds. Appl Environ Microb 68:4283–4291. doi:10.1128/Aem.68.9.4283-4291.2002
80. Kralj S, Van Geel-Schutten GH, Dondorff MMG, Kirsanovs S, Van Der Maarel MJEC, Dijkhuizen L (2004) Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiol-Sgm 150:3681–3690. doi:10.1099/Mic.0.27321-0
81. Kruse HP, Kleessen B, Blaut M (1999) Effects of inulin on faecal bifidobacteria in human subjects. Brit J Nutr 82:375–382
82. Kumar AS, Mody K, Jha B (2007) Bacterial exopolysaccharides—a perception. J Basic Microbiol 47:103–117
83. Lacaze G, Wick M, Cappelle S (2007) Emerging fermentation technologies: development of novel sourdoughs. Food Microbiol 24:155–160. doi:10.1016/J.Fm.2006.07.015
84. Laws A, Gu Y, Marshall V (2001) Biosynthesis, characterisation, and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnol Adv 19:597–625. doi:10.1016/S0734-9750(01)00084-2
85. Leathers T (2002) Dextran. In: Steinbüchel Sab A, Vandamme EH (eds) Biopolymers. Wiley Vch, Weinheim, pp 299–322
86. Leathers TD, Hayman GT, Côté GL (1995) Rapid screening of Leuconostoc mesenteroides mutants for elevated proportions of alternan to dextran. Curr Microbiol 31:19–22. doi:10.1007/Bf00294628
87. Leathers TD, Ahlgren JA, Côté GL (1997) Alternansucrase mutants of Leuconostoc mesenteroides strain NRRL B-21138. J Ind Microbiol Biot 18:278–283. doi:10.1038/Sj.Jim.2900380
88. Leathers TD, Nunnally MS, Ahlgren JA, Côté GL (2003) Characterization of a novel modified alternan. Carbohyd Polym 54:107–113. doi:10.1016/S0144-8617(03)00157-7
89. Leathers TD, Nunnally MS, Côté GL (2010) Optimization of process conditions for enzymatic modification of alternan using dextranase from Chaetomium erraticum. Carbohyd Polym 81:732–736. doi:10.1016/J.Carbpol.2010.03.030
90. Leemhuis H, Pijning T, Dobruchowska JM, Van Leeuwen SS, Kralj S, Dijkstra BW, Dijkhuizen L (2013) Glucansucrases: three-dimensional structures, reactions, mechanism, α-glucan analysis and their implications in biotechnology and food applications. J Biotechnol 163:250–272. doi:10.1016/J.Jbiotec.2012.06.037
91. Lemieux P, Precourt LP, Simard E (2006) Use of Lactobacillus kefiranofaciens as a probiotic and a synbiotic. Patent N. Us20140193383 A1.
92. Liu C, Lu J, Lu L, Liu Y, Wang F, Xiao M (2010) Isolation, structural characterization and immunological activity of an exopolysaccharide produced by Bacillus licheniformis 8-37-0-1. Bioresour Technol 101:5528–5533. doi:10.1016/J.Biortech.2010.01.151
93. Looijesteijn PJ, Van Casteren WHM, Tuinier R, Doeswijk-Voragen CHL, Hugenholtz J (2000) Influence of different substrate limitations on the yield, composition and molecular mass of exopolysaccharides produced by Lactococcus lactis subsp cremoris in continuous cultures. J Appl Microbiol 89:116–122. doi:10.1046/J.1365-2672.2000.01082.X
94. Looijesteijn PJ, Trapet L, De Vries E, Abee T, Hugenholtz J (2001) Physiological function of exopolysaccharides produced by Lactococcus lactis. Int J Food Microbiol 64:71–80. doi:10.1016/S0168-1605(00)00437-2
95. Maeda H, Zhu X, Omura K, Suzuki S, Kitamura S (2004) Effects of an exopolysaccharide (kefiran) on lipids, blood pressure, blood glucose, and constipation. Biofactors 22:197–200
96. Marx SP, Winkler S, Hartmeier W (2000) Metabolization of beta-(2,6)-linked fructose-oligosaccharides by different bifidobacteria. FEMS Microbiol Lett 182:163–169. doi:10.1111/J.1574-6968.2000.Tb08891.X
97. Masco L, Huys G, De Brandt E, Temmerman R, Swings J (2005) Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol 102:221–230. doi:10.1016/J.Ijfoodmicro.2004.11.018
98. McCurdy RD, Goff HD, Stanley DW, Stone AP (1994) Rheological properties of dextran related to food applications. Food Hydrocolloid 8:609–623. doi:10.1016/S0268-005x(09)80068-4
99. Melo IR, Pimentel MF, Lopes CE, Calazans GMT (2007) Application of fractional factorial design to levan production by Zymomonas mobilis. Braz J Microbiol 38:45–51
100. Meng X, Dobruchowska JM, Gerwig GJ, Kamerling JP, Dijkhuizen L (2015) Synthesis of oligo- and polysaccharides by Lactobacillus reuteri 121 reuteransucrase at high concentrations of sucrose. Carbohyd Res 414:85–92. doi:10.1016/J.Carres.2015.07.011
101. Micheli L, Uccelletti D, Palleschi C, Crescenzi V (1999) Isolation and characterisation of a ropy Lactobacillus strain producing the exopolysaccharide kefiran. Appl Microbiol Biot 53:69–74. doi:10.1007/S002530051616
102. Monsan P, Bozonnet S, Albenne C, Joucla G, Willemot RM, Remaud-Simeon M (2001) Homopolysaccharides from lactic acid bacteria. Int Dairy J 11:675–685. doi:10.1016/S0958-6946(01)00113-3
103. Mora-Gutierrez A (2014) Compositions for targeted anti-aging therapy. Patent N. Wo2014028585 A1
104. Naessens M, Cerdobbel A, Soetaert W, Vandamme EJ (2005) Leuconostoc dextransucrase and dextran: production, properties and applications. J Chem Technol Biotechnol 80:845–860. doi:10.1002/Jctb.1322
105. Neely WB, Nott J (1962) Dextransucrase, an induced enzyme from Leuconostoc mesenteroides. Biochemistry 1:1136–1140. doi:10.1021/Bi00912a027
106. Novak LJ (1957) Food Preservation. Patent N. Us2790720 A, New York
107. Nwodo U, Green E, Okoh A (2012) Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci 13:14002–14015
108. Olivares-Illana V, López-Munguía A, Olvera C (2003) Molecular characterization of inulosucrase from Leuconostoc citreum: a fructosyltransferase within a glucosyltransferase. J Bacteriol 185:3606–3612. doi:10.1128/Jb.185.12.3606-3612.2003
109. Orla-Jensen S (1943) The lactic acid bacteria vol 3. Biologiske Skrifter Bind Ii, Kopenhagen
110. Park JS (2007) Functional chewing gum composition for improving effectively obesity and blood fat. China Patentn. Cn1311836 C
111. Park HO, Bang YB, Joung HJ, Kim BC, Kim HR (2004) Lactobacillus for use in the treatment of eating disorders and pancreatic defects. Patent N. Ep2392340 B1
112. Paseephol T, Small DM, Sherkat F (2008) Rheology and texture of set yogurt as affected by inulin addition. J Texture Stud 39:617–634
113. Pasteur L (1861) Sur la fermentation visqueuse bulletin de la société de chimie: 30–31
114. Patel Ap JB (2013) Food and health applications of exopolysaccharides produced by lactic acid bacteria. Adv Dairy Res 1:1–7. doi:10.4172/2329-888x.1000107
115. Patel AK, Michaud P, Singhania RR, Soccol CR, Pandey A (2010) Polysaccharides from probiotics: new developments as food additives. Food Technol Biotech 48:451–463
116. Patel S, Majumder A, Goyal A (2012) Potentials of exopolysaccharides from lactic acid bacteria. Indian J Microbiol 52:3–12. doi:10.1007/S12088-011-0148-8
117. Pham PL, Dupont I, Roy D, Lapointe G, Cerning J (2000) Production of exopolysaccharide by Lactobacillus rhamnosus R and analysis of its enzymatic degradation during prolonged fermentation. Appl Environ Microb 66:2302–2310. doi:10.1128/Aem.66.6.2302-2310.2000
118. Pidoux M (1989) The microbial flora of sugary kefir grain (the gingerbeer plant): biosynthesis of the grain from Lactobacillus hilgardii producing a polysaccharide gel. MIRCEN J Appl Microbiol Biotechnol 5:223–238. doi:10.1007/Bf01741847
119. Pidoux M, Brillouet JM, Quemener B (1988) Characterization of the polysaccharides from a Lactobacillus brevis and from sugary kefir grains. Biotechnol Lett 10:415–420. doi:10.1007/Bf01087442
120. Pidoux M, De Ruiter GA, Brooker BE, Colquhoun IJ, Morris VJ (1990) Microscopic and chemical studies of a gelling polysaccharide from Lactobacillus hilgardii. Carbohyd Polym 13:351–362. doi:10.1016/0144-8617(90)90035-Q
121. Piermaria JA, Pinotti A, Garcia MA, Abraham AG (2009) Films based on kefiran, an exopolysaccharide obtained from kefir grain: development and characterization. Food Hydrocolloid 23:684–690. doi:10.1016/J.Foodhyd.2008.05.003
122. Pleszczyńska M, Wiater A, Janczarek M, Szczodrak J (2015) (1→3)-α-d-Glucan hydrolases in dental biofilm prevention and control: a review. Int J Biol Macromol 79:761–778. doi:10.1016/J.Ijbiomac.2015.05.052
123. Pool-Zobel BL (2005) Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data. Brit J Nutr 93:S73–S90. doi:10.1079/Bjn20041349
124. Pucci MJ, Kunka BS (1990) Novel dextran produced by Leuconostoc dextranicum. Patent N. Us4933191 A
125. Ravyts F, De Vuyst LUC, Leroy F (2011) The effect of heteropolysaccharide-producing strains of Streptococcus thermophilus on the texture and organoleptic properties of low-fat yoghurt. Int J Dairy Technol 64:536–543. doi:10.1111/J.1471-0307.2011.00714.X
126. Rodrigues KL, Caputo LRG, Carvalho JCT, Evangelista J, Schneedorf JM (2005) Antimicrobial and healing activity of kefir and kefiran extract. Int J Antimicrob Agents 25:404–408. doi:10.1016/J.Ijantimicag.2004.09.020
127. Rohm H, Kovac A (1994) Effects of starter cultures on linear viscoelastic and physical properties of yogurt gels. J Texture Stud 25:311–329
128. Rohm H, Schmid W (1993) Influence of dry matter fortification on flow properties of yogurt. Eval Flow Curves Milchwissenschaft 48:556–560
129. Rosell KG, Birkhed D (1974) An inulin-like fructan produced by Streptococcus mutans, strain JC2. Acta Chem Scand B 28:589
130. Ruas-Madiedo P, de los Reyes-Gavilan CG (2005) Invited review: methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J Dairy Sci 88:843–856
131. Ruas-Madiedo PSN, de los Reyes-Gavilan CG (2009) Biosynthesis and chemical composition of exopolysaccharides produced by lactic acid bacteri in bacterial polysaccharides. In: Ullrich M (ed) Bacterial polysaccharides: current innovations and future trends. Caister Academic Press, UK
132. Ruas-Madiedo P, Hugenholtz J, Zoon P (2002) An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int Dairy J 12:163–171. doi:10.1016/S0958-6946(01)00160-1
133. Rühmann B, Schmid J, Sieber V (2015) Methods to identify the unexplored diversity of microbial exopolysaccharides. Front Microbiol 6:565. doi:10.3389/Fmicb.2015.00565
134. Russo P, López P, Capozzi V, de Palencia PF, Dueñas MT, Spano G, Fiocco D (2012) Beta-Glucans improve growth, viability and colonization of probiotic microorganisms. Int J Mol Sci 13:6026
135. Ryan PM, Ross RP, Fitzgerald GF, Caplice NM, Stanton C (2015) Sugar-coated: exopolysaccharide producing lactic acid bacteria for food and human health applications. Food Funct 6:679–693. doi:10.1039/C4fo00529e
136. Salazar N, Gueimonde M, Hernandez-Barranco AM, Ruas-Madiedo P, Reyes-Gavilan CGDL (2008) Exopolysaccharides produced by intestinal Bifidobacterium Strains act as fermentable substrates for human intestinal bacteria. Appl Environ Microb 74:4737–4745. doi:10.1128/Aem.00325-08
137. Salazar N, Gueimonde M, De Los Reyes-Gavilán CG, Ruas-Madiedo P (2015) Exopolysaccharides produced by Lactic acid bacteria and bifidobacteria as fermentable substrates by the intestinal microbiota. Critical Reviews in Food Science and Nutrition: 00–00 doi:10.1080/10408398.2013.770728
138. Sartor RB (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126:1620–1633
139. Schwab C, Walter J, Tannock GW, Vogel RF, Gänzle MG (2007) Sucrose utilization and impact of sucrose on glycosyltransferase expression in Lactobacillus reuteri. Syst Appl Microbiol 30:433–443. doi:10.1016/J.Syapm.2007.03.007
140. Seibel J, Buchholz K (2010) Tools in oligosaccharide synthesis current research and application. Adv Carbohydr Chem Biochem 63:101–138. doi:10.1016/S0065-2318(10)63004-1
141. Shiroza T, Kuramitsu HK (1988) Sequence analysis of the Streptococcus mutans fructosyltransferase gene and flanking regions. J Bacteriol 170:810–816
142. Sletmoen M, Stokke BT (2008) Higher order structure of (1,3)-β-d-glucans and its influence on their biological activities and complexation abilities. Biopolymers 89:310–321. doi:10.1002/Bip.20920
143. Smith MR, Zahnley J, Goodman N (1994) Glucosyltransferase mutants of Leuconostoc mesenteroides NRRL B-1355. Appl Environ Microbiol 60:2723–2731
144. Smith MR, Zahnley JC, Wong RY, Lundin RE, Ahlgren JA (1998) A mutant strain of Leuconostoc mesenteroides b-1355 producing a glucosyltransferase synthesizing alpha(1->2) glucosidic linkages. J Ind Microbiol Biot 21:37–45. doi:10.1038/Sj.Jim.2900558
145. Song KB, Bae KS, Lee YB, Lee KY, Rhee SK (2000) Characteristics of levan fructotransferase from Arthrobacter ureafaciens K2032 and difructose anhydride IV formation from levan. Enzyme Microb Tech 27:212–218
146. Stanton C, Ross P, Fitzgerald GF, Caplice N, Shanahan F (2014) Exopolysaccharide-producing bacteria, and uses thereof for protecting heart health. Patents No. Wo2014033307 A1
147. Surayot U, Wang J, Seesuriyachan P, Kuntiya A, Tabarsa M, Lee Y, Kim JK, Park W, You S (2014) Exopolysaccharides from lactic acid bacteria: structural analysis, molecular weight effect on immunomodulation. Int J Biol Macromol 68:233–240. doi:10.1016/J.Ijbiomac.2014.05.005
148. Tárrega A, Costell E (2006) Effect of inulin addition on rheological and sensory properties of fat-free starch-based dairy desserts. Int Dairy J 16:1104–1112
149. Tieking M, Ganzle MG (2005) Exopolysaccharides from cereal-associated lactobacilli. Trends Food Sci Tech 16:79–84. doi:10.1016/J.Tifs.2004.02.015
150. Tieking M, Korakli M, Ehrmann MA, Gänzle MG, Vogel RF (2003) In situ production of exopolysaccharides during sourdough fermentation by cereal and intestinal isolates of lactic acid bacteria. Appl Environ Microb 69:945–952. doi:10.1128/Aem.69.2.945-952.2003
151. Tieking M, Kuhnl W, Ganzle MG (2005) Evidence for formation of heterooligosaccharides by Lactobacillus sanfranciscensis during growth in wheat sourdough. J Agr Food Chem 53:2456–2461. doi:10.1021/Jf048307v
152. Torino MI, Sesma F, Font de Valdez G (2000) Semi-defined media for the exopolysaccharide (EPS) production by Lactobacillus helveticus ATCC 15807 and evaluation of the components interfering with the EPS quantification. Milchwissenschaft 55:314–316
153. Torino MI, Font De Valdez G, Mozzi F (2015) Biopolymers from lactic acid bacteria. novel applications in foods and beverages. Front Microbiol 6:834. doi:10.3389/Fmicb.2015.00834
154. Ullrich M (2009) Commercial exploitation of homo-exopolysaccharides in non-dairy food systems. In Bacterial Polysaccharides: Current Innovations and Future Trends. Caister Academic Press, Norfolk
155. Uzochukwu S, Balogh E, Loefler RT, Ngoddy PO (2001) Structural analysis by 13C-nuclear magnetic resonance spectroscopy of glucans elaborated by gum-producing bacteria isolated from palm wine. Food Chem 73:225–233. doi:10.1016/S0308-8146(00)00291-0
156. Van Geel-Schutten GH (2006) Use of a polysaccharide as bread improver. Patent No. Wo2006062410 A1
157. Van Geel-Schutten GH, Flesch F, Ten Brink B, Smith MR, Dijkhuizen L (1998) Screening and characterization of Lactobacillus strains producing large amounts of exopolysaccharides. Appl Microbiol Biot 50:697–703
158. Van Hijum SAFT, Bonting K, Van Der Maarel MJEC, Dijkhuizen L (2001) Purification of a novel fructosyltransferase from Lactobacillus reuteri strain 121 and characterization of the levan produced. FEMS Microbiol Lett 205:323–328. doi:10.1016/S0378-1097(01)00490-6
159. Van Hijum SAFT, Szalowska E, Van Der Maarel M, Dijkhuizen L (2004) Biochemical and molecular characterization of a levansucrase from Lactobacillus reuteri. Microbiol-Sgm 150:621–630. doi:10.1099/Mic.0.26671-0
160. Van Hijum SAFT, Kralj S, Ozimek LK, Dijkhuizen L, Van Geel-Schutten IGH (2006) Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 70:157–176. doi:10.1128/Mmbr.70.1.157-176.2006
161. Van Leeuwen SS, Kralj S, Van Geel-Schutten IH, Gerwig GJ, Dijkhuizen L, Kamerling JP (2008) Structural analysis of the α-d-glucan (EPS35-5) produced by the Lactobacillus reuteri strain 35-5 glucansucrase GTFA enzyme. Carbohyd Res 343:1251–1265. doi:10.1016/J.Carres.2008.01.044
162. Van Leeuwen SS, Kralj S, Eeuwema W, Gerwig GJ, Dijkhuizen L, Kamerling JP (2009) Structural characterization of bioengineered α-d-glucans produced by mutant glucansucrase GTF180 enzymes of Lactobacillus reuteri strain 180. Biomacromolecules 10:580–588. doi:10.1021/Bm801240r
163. Vandamme E, Renard CEFG, Arnaut FRJ, Vekemans NMF, Tossut PPA (2002a) Process for obtaining improved structure build-up of baked products. Patent No Us 6 399 119, Weinheim
164. Vandamme EJ, De Baets S, Steinbuchel A, De Baets S (2002b) Alternan. In: Vandamme EJ, Steinbuchel A (eds) Biopolymers polysaccharides i: polysaccharides from prokaryotes, vol 5. Wiley, Weinheim, pp 323–350
165. Vijn I, Smeekens S (1999) Fructan: more than a reserve carbohydrate? Plant Physiol 120:351–359
166. Vincent S, Brandt M, Cavadini C, Hammes WP, Neeser JR, Waldbuesser S (2005) Levan-producing Lactobacillus strain and method of preparing human or pet products using the same. Patent No. Us 2004/0005348 A1
167. Von Wright A, Axelsson L (2012) Lactic acid bacteria: An introduction. In: Sampo Lahtinen Acossavw (Ed) Lactic Acid Bacteria: Microbiological and functional aspects, Fourth Edition. Crc Press, New York
168. Waldherr FW, Doll VM, Meißner D, Vogel RF (2010) Identification and characterization of a glucan-producing enzyme from Lactobacillus hilgardii TMW 1.828 involved in granule formation of water kefir. Food Microbiol 27:672–678. doi:10.1016/J.Fm.2010.03.013
169. Walter J, Schwab C, Loach DM, Gänzle MG, Tannock GW (2008) Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology 154:72–80. doi:10.1099/Mic.0.2007/010637-0
170. Wang X, Gibson GR (1993) Effects of the in-vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol 75:373–380. doi:10.1111/J.1365-2672.1993.Tb02790.X
171. Ward HM (1892) The ginger-beer plant, and the organisms composing it: a contribution to the study of fermentation-yeasts and bacteria. Philos Trans R Soc Lond B Biol Sci 183:125–197. doi:10.1098/Rstb.1892.0006
172. Werning ML, Ibarburu I, Duenas MT, Irastorza A, Navas J, Lopez P (2006) Pediococcus parvulus GTF gene encoding the GTF glycosyltransferase and its application for specific PCR detection of beta-d-glucan-producing bacteria in foods and beverages. J Food Protect 69:161–169
173. William MP, Joseph U (1959) Use of dextran in freeze-drying process. Patent No. Us2908614a
174. Yoo S-H, Yoon EJ, Cha J, Lee HG (2004) Antitumor activity of levan polysaccharides from selected microorganisms. Int J Biol Macromol 34:37–41. doi:10.1016/J.Ijbiomac.2004.01.002
175. Zahnley JC, Smith MR (1995) Insoluble glucan formation by Leuconostoc mesenteroides B-1355. Appl Environ Microb 61:1120–1123
176. Zannini E, Mauch A, Galle S, Gänzle M, Coffey A, Arendt EK, Taylor JP, Waters DM (2013) Barley malt wort fermentation by exopolysaccharide-forming Weissella cibaria MG1 for the production of a novel beverage. J Appl Microbiol 115(6):1379–1387. doi:10.1111/Jam.12329
177. Zhang L, Li X, Xu X, Zeng F (2005) Correlation between antitumor activity, molecular weight, and conformation of lentinan. Carbohyd Res 340:1515–1521. doi:10.1016/J.Carres.2005.02.032