Influence of levan-producing acetic acid bacteria on buckwheat-sourdough breads

Food Microbiology

Volumn 65, Issue , 2017, Pages 95-104

  Ua Arak, Tharalinee ^a   Jakob, Frank ^a   Vogel, Rudi F ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Acetic acid bacteria; Buckwheat; Field flow fractionation; Fructan; Gluten free; Sourdough

Indexed keywords

ACETIC ACID; ANTINEOPLASTIC AGENT; FRUCTAN; GLUTEN; LEVAN;

ACETOBACTERACEAE; ANALYSIS; BACTERIUM; BIOSYNTHESIS; BREAD; FAGOPYRUM; FERMENTATION; FLOUR; FOOD CONTROL; GLUCONOBACTER; GROWTH, DEVELOPMENT AND AGING; LACTOBACILLACEAE; METABOLISM; MICROBIOLOGY;

ACETIC ACID; ACETOBACTERACEAE; ANTINEOPLASTIC AGENTS; BACTERIA; BREAD; FAGOPYRUM; FERMENTATION; FLOUR; FOOD MICROBIOLOGY; FRUCTANS; GLUCONOBACTER; GLUTENS; LACTOBACILLACEAE;

EID: 85012048857     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2017.02.002     Document Type: Article

References (75)

1. Adachi, O., Matsushita, K., Shinagawa, E., Ameyama, M., Occurrence of old yellow enzyme in Gluconobacter suboxydans, and the cyclic regeneration of NADP. J. Biochem. 86 (1979), 699–709.
2. Anton, A.A., Artfield, S.D., Hydrocolloids in gluten-free breads: a review. Int. J. Food Sci. Nutr. 59 (2008), 11–23.
3. Arendt, E.K., Ryan, L.A., Dal Bello, F., Impact of sourdough on the texture of bread. Food Microbiol. 24 (2007), 165–174.
4. Arvidson, S.A., Rinehart, B.T., Gadala-Maria, F., Concentration regimes of solutions of levan polysaccharide from Bacillus sp. Carbohydr. Polym. 65 (2006), 144–149.
5. Bakr, A.A., Production of iron-fortified bread employing some selected natural iron sources. Food Nahr. 41 (1997), 293–298.
6. Barber, B., Ortolá, C., Barber, S., Fernández, F., Storage of packaged white bread - III. Effects of sour dough and addition of acids on bread characteristics. Z. für Lebensm. Forschung 194 (1992), 442–449.
7. Benigar, E., Dogsa, I., Stopar, D., Jamnik, A., Cigić, I.K., Tomšič, M., Structure and dynamics of a polysaccharide matrix: aqueous solutions of bacterial levan. Langmuir 30 (2014), 4172–4182.
8. Brandt, M., 2013. Einsatz von Essigsäurebakterien zur Herstellung von Backwaren, European patent, WO2013113602 A2 ed.
9. Campo, E., del Arco, L., Urtasun, L., Oria, R., Ferrer-Mairal, A., Impact of sourdough on sensory properties and consumers’ preference of gluten-free breads enriched with teff flour. J. Cereal Sci. 67 (2016), 75–82.
10. Capriles, V.D., Arêas, J.A.G., Novel approaches in gluten-free breadmaking: interface between food science, nutrition, and health. Compr. Rev. Food Sci. Food Saf. 13 (2014), 871–890.
11. Chaves-Lopez, C., Serio, A., Delgado-Ospina, J., Rossi, C., Grande-Tovar, C.D., Paparella, A., Exploring the bacterial microbiota of colombian fermented maize dough “Masa agria” (Maiz añejo). Front. Microbiol. 7 (2016), 1–12.
12. Corsetti, A., Gobbetti, M., Rossi, J., Damiani, P., Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Appl. Microbiol. Biotechnol. 50 (1998), 253–256.
13. Corsetti, A., Settanni, L., Lactobacilli in sourdough fermentation. Food Res. Int. 40 (2007), 539–558.
14. Costantini, L., Lukšič, L., Molinari, R., Kreft, I., Bonafaccia, G., Manzi, L., Merendino, N., Development of gluten-free bread using tartary buckwheat and chia flour rich in flavonoids and omega-3 fatty acids as ingredients. Food Chem. 165 (2014), 232–240.
15. Czerny, M., Schieberle, P., Important aroma compounds in freshly ground wholemeal and white wheat flour - identification and quantitative changes during sourdough fermentation. J. Agric. Food Chem. 50 (2002), 6835–6840.
16. De Vuyst, L., Neysens, P., The sourdough microflora: biodiversity and metabolic interactions. Trends Food Sci. Technol. 16 (2005), 43–56.
17. Deppenmeier, U., Hoffmeister, M., Prust, C., Biochemistry and biotechnological applications of Gluconobacter strains. Appl. Microbiol. Biotechnol. 60 (2002), 233–242.
18. Duetz, W.A., Witholt, B., Oxygen transfer by orbital shaking of square vessels and deepwell microtiter plates of various dimensions. Biochem. Eng. J. 17 (2004), 181–185.
19. Filipcev, P., Sugar beet molasses: an ingredient to enhance micronutrients and funtionality in bread. Food Feed Res. 38 (2011), 95–100.
20. Galle, S., Schwab, C., Arendt, E., Ganzle, M., Exopolysaccharide-forming Weissella strains as starter cultures for sorghum and wheat sourdoughs. J. Agric. Food Chem. 58 (2010), 5834–5841.
21. Galle, S., Schwab, C., Dal Bello, F., Coffey, A., Ganzle, M.G., Arendt, E.K., Influence of in-situ synthesized exopolysaccharides on the quality of gluten-free sorghum sourdough bread. Int. J. Food Microbiol. 155 (2012), 105–112.
22. Gänzle, M.G., Ehmann, M., Hammes, W.P., Modeling of growth of Lactobacillus sanfranciscensis and Candida milleri in response to process parameters of sourdough fermentation. Appl. Environ. Microbiol. 64 (1998), 2616–2623.
23. Garay-Arroyo, A., Covarrubias, A.A., Clark, I., Niño, I., Gosset, G., Martinez, A., Response to different environmental stress conditions of industrial and laboratory Saccharomyces cerevisiae strains. Appl. Microbiol. Biotechnol. 63 (2004), 734–741.
24. Garcia-Ochoa, F., Gomez, E., Bioreactor scale-up and oxygen transfer rate in microbial processes: an overview. Biotechnol. Adv. 27 (2009), 153–176.
25. Gobbetti, M., Rizzello, C.G., Di Cagno, R., De Angelis, M., How the sourdough may affect the functional features of leavened baked goods. Food Microbiol. 37 (2014), 30–40.
26. Graves, T., Narendranath, N.V., Dawson, K., Power, R., Interaction effects of lactic acid and acetic acid at different temperatures on ethanol production by Saccharomyces cerevisiae in corn mash. Appl. Microbiol. Biotechnol. 73 (2007), 1190–1196.
27. Hager, A.-S., Arendt, E.K., Influence of hydroxypropylmethylcellulose (HPMC), xanthan gum and their combination on loaf specific volume, crumb hardness and crumb grain characteristics of gluten-free breads based on rice, maize, teff and buckwheat. Food Hydrocoll. 32 (2013), 195–203.
28. Hammes, W.P., Gänzle, M.G., Sourdough breads and related products. Wood, B.J.B., (eds.) Microbiology of Fermented Foods, 1997, Springer US, Boston, MA, 199–216.
29. Hermann, M., Petermeier, H., Vogel, R., Development of novel sourdoughs with in situ formed exopolysaccharides from acetic acid bacteria. Eur. Food Res. Technol., 2015, 1–13.
30. Jakob, F., Pfaff, A., Novoa-Carballal, R., Rubsam, H., Becker, T., Vogel, R.F., Structural analysis of fructans produced by acetic acid bacteria reveals a relation to hydrocolloid function. Carbohydr. Polym. 92 (2013), 1234–1242.
31. Jakob, F., Steger, S., Vogel, R.F., Influence of novel fructans produced by selected acetic acid bacteria on the volume and texture of wheat breads. Eur. Food Res. Technol. 234 (2012), 493–499.
32. Kaditzky, S., Seitter, M., Hertel, C., Vogel, R.F., Performance of Lactobacillus sanfranciscensis TMW 1.392 and its levansucrase deletion mutant in wheat dough and comparison of their impact on bread quality. Eur. Food Res. Technol. 227 (2008), 433–442.
33. Kern, C.C., Usbeck, J.C., Vogel, R.F., Behr, J., Optimization of matrix-assisted-laser-desorption–ionization-time-of-flight mass spectrometry for the identification of bacterial contaminants in beverages. J. Microbiol. Methods 93 (2013), 185–191.
34. Kim, M.G., Seo, J.W., Song, K.B., Kim, C.H., Chung, B.H., Rhee, S.K., Levan and fructosyl derivatives formation by a recombinant levansucrase from Rahnella aquatilis. Biotechnol. Lett. 20 (1998), 333–336.
35. Kitamura, S., Hirano, T., Takeo, K., Mimura, M., Kajiwara, K., Stokke, B.T., Harada, T., Conformation of (2→1)-β-d-fructan in aqueous solution. Int. J. Biol. Macromol. 16 (1994), 313–317.
36. Konitzer, K., Pflaum, T., Oliveira, P., Arendt, E., Koehler, P., Hofmann, T., Kinetics of sodium release from wheat bread crumb as affected by sodium distribution. J. Agric. Food Chem. 61 (2013), 10659–10669.
37. Korakli, M., Rossmann, A., Gänzle, M.G., Vogel, R.F., Sucrose metabolism and exopolysaccharide production in wheat and rye sourdoughs by Lactobacillus sanfranciscensis. J. Agric. Food Chem. 49 (2001), 5194–5200.
38. Lavermicocca, P., Valerio, F., Evidente, A., Lazzaroni, S., Corsetti, A., Gobbetti, M., Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl. Environ. Microbiol. 66 (2000), 4084–4090.
39. Lazaridou, A., Duta, D., Papageorgiou, M., Belc, N., Biliaderis, C.G., Effects of hydrocolloids on dough rheology and bread quality parameters in gluten-free formulations. J. Food Eng. 79 (2007), 1033–1047.
40. Lilley, B.D., Brewer, J.H., The selective antibacterial action of phenylethyl alcohol. J. Am. Pharm. Assoc. 42 (1953), 6–8.
41. Macauley, S., McNeil, B., Harvey, L.M., The genus Gluconobacter and its applications in biotechnology. Crit. Rev. Biotechnol. 21 (2001), 1–25.
42. Méndez-Lorenzo, L., Porras-Domínguez, J.R., Raga-Carbajal, E., Olvera, C., Rodríguez-Alegría, M.E., Carrillo-Nava, E., Costas, M., Munguía, A.L., Intrinsic levanase activity of Bacillus subtilis 168 levansucrase (SacB). PLoS One, 10, 2015.
43. Menéndez, C., Hernández, L., Selman, G., Mendoza, M.F., Hevia, P., Sotolongo, M., Arrieta, J.G., Molecular cloning and expression in Escherichia coli of an exo-levanase gene from the endophytic bacterium Gluconacetobacter diazotrophicus SRT4. Curr. Microbiol. 45 (2002), 5–12.
44. Minervini, F., Lattanzi, A., De Angelis, M., Di Cagno, R., Gobbetti, M., Influence of artisan bakery- or laboratory-propagated sourdoughs on the diversity of lactic acid bacterium and yeast microbiotas. Appl. Environ. Microbiol. 78 (2012), 5328–5340.
45. Moroni, A.V., Arendt, E.K., Bello, F.D., Biodiversity of lactic acid bacteria and yeasts in spontaneously-fermented buckwheat and teff sourdoughs. Food Microbiol. 28 (2011), 497–502.
46. Moroni, A.V., Dal Bello, F., Arendt, E.K., Sourdough in gluten-free bread-making: an ancient technology to solve a novel issue?. Food Microbiol. 26 (2009), 676–684.
47. Moroni, A.V., Zannini, E., Sensidoni, G., Arendt, E.K., Exploitation of buckwheat sourdough for the production of wheat bread. Eur. Food Res. Technol. 235 (2012), 659–668.
48. Newbrun, E., Lacy, R., Christie, T.M., The morphology and size of the extracellular polysaccharides from oral streptococci. Arch. Oral Biol. 16 (1971), 863–872.
49. Öner, E.T., Hernández, L., Combie, J., Review of levan polysaccharide: from a century of past experiences to future prospects. Biotechnol. Adv. 34 (2016), 827–844.
50. Pampulha, M.E., Loureiro-Dias, M.C., Energetics of the effect of acetic acid on growth of Saccharomyces cerevisiae. FEMS Microbiol. Lett. 184 (2000), 69–72.
51. Raspor, P., Goranovic, D., Biotechnological applications of acetic acid bacteria. Crit. Rev. Biotechnol. 28 (2008), 101–124.
52. Richhardt, J., Bringer, S., Bott, M., Role of the pentose phosphate pathway and the Entner-Doudoroff pathway in glucose metabolism of Gluconobacter oxydans 621H. Appl. Microbiol. Biotechnol. 97 (2013), 4315–4323.
53. Ronda, F., Villanueva, M., Collar, C., Influence of acidification on dough viscoelasticity of gluten-free rice starch-based dough matrices enriched with exogenous protein. LWT Food Sci. Technol. 59 (2014), 12–20.
54. Rózylo, R., Rudy, S., Krzykowski, A., Dziki, D., Gawlik-Dziki, U., Rózylo, K., Skonecki, S., Effect of adding fresh and freeze-dried buckwheat sourdough on gluten-free bread quality. Int. J. Food Sci. Technol. 50 (2015), 313–322.
55. Rühmkorf, C., Jungkunz, S., Wagner, M., Vogel, R.F., Optimization of homoexopolysaccharide formation by lactobacilli in gluten-free sourdoughs. Food Microbiol. 32 (2012), 286–294.
56. Rühmkorf, C., Rübsam, H., Becker, T., Bork, C., Voiges, K., Mischnick, P., Brandt, M.J., Vogel, R.F., Effect of structurally different microbial homoexopolysaccharides on the quality of gluten-free bread. Eur. Food Res. Technol. 235 (2012), 139–146.
57. Runyon, J.R., Nilsson, L., Ulmius, M., Castro, A., Ionescu, R., Andersson, C., Schmidt, C., Characterizing changes in levan physicochemical properties in different pH environments using asymmetric flow field-flow fractionation. Anal. Bioanal. Chem. 406 (2014), 1597–1605.
58. Sabanis, D., Tzia, C., Effect of hydrocolloids on selected properties of gluten-free dough and bread. Food Sci. Technol. Int. 17 (2011), 279–291.
59. Scheirlinck, I., Van Der Meulen, R., Van Schoor, A., Vancanneyt, M., De Vuyst, L., Vandamme, P., Huys, G., Taxonomic structure and stability of the bacterial community in Belgian sourdough ecosystems as assessed by culture and population fingerprinting. Appl. Environ. Microbiol. 74 (2008), 2414–2423.
60. Schwab, C., Mastrangelo, M., Corsetti, A., Gänzle, M., Formation of oligosaccharides and polysaccharides by Lactobacillus reuteri LTH5448 and Weissella cibaria 10M in sorghum sourdoughs. Cereal Chem. 85 (2008), 679–684.
61. Sciarini, L.S., Ribotta, P.D., León, A.E., Pérez, G.T., Effect of hydrocolloids on gluten-free batter properties and bread quality. Int. J. Food Sci. Technol. 45 (2010), 2306–2312.
62. Sengun, I.Y., Karabiyikli, S., Importance of acetic acid bacteria in food industry. Food Control. 22 (2011), 647–656.
63. Simurina, O.D., Ikonic, B.B., Jevtic−Mucibabic, R.C., Belovic, M.M., Koprivica, G.B., Misljenovic, N.M., Application of reponse surface methodology in the development of specialty bread with sugar beet molasses, flax seed and vital wheat gluten. Food Feed Res. 39 (2012), 11–21.
64. Spicher, G., The microflora of sourdough - XXII. Communication: the lactobacillus species of wheat sourdough. Z. für Lebensm. Forschung 184 (1987), 300–303.
65. Srikanth, R., Reddy, C.H.S.S.S., Siddartha, G., Ramaiah, M.J., Uppuluri, K.B., Review on production, characterization and applications of microbial levan. Carbohydr. Polym. 120 (2015), 102–114.
66. Stolz, P., Böcker, G., Hammes, W.P., Vogel, R.F., Utilization of electron acceptors by lactobacilli isolated from sourdough - I. Lactobacillus sanfrancisco. Z. für Lebensm. Forschung 201 (1995), 91–96.
67. Suzuki, T., Morishita, T., Mukasa, Y., Takigawa, S., Yokota, S., Ishiguro, K., Noda, T., Breeding of ‘Manten-Kirari’, a non-bitter and trace-rutinosidase variety of tartary buckwheat (Fagopyrum tataricum Gaertn.). Breed. Sci. 64 (2015), 344–350.
68. Taherzadeh, M.J., Niklasson, C., Lidén, G., Acetic acid-friend or foe in anaerobic batch conversion of glucose to ethanol by Saccharomyces cerevisiae?. Chem. Eng. Sci. 52 (1997), 2653–2659.
69. Thompson, T., Folate, iron, and dietary fiber contents of the gluten-free diet. J. Am. Diet. Assoc. 100 (2000), 1389–1396.
70. Tieking, M., Korakli, M., Ehrmann, M.A., Ganzle, M.G., Vogel, R.F., In situ production of exopolysaccharides during sourdough fermentation by cereal and intestinal isolates of lactic acid bacteria. Appl. Environ. Microbiol. 69 (2003), 945–952.
71. Torbica, A., Hadnađev, M., Dapčević, T., Rheological, textural and sensory properties of gluten-free bread formulations based on rice and buckwheat flour. Food Hydrocoll. 24 (2010), 626–632.
72. Ua-Arak, T., Jakob, F., Vogel, R.F., Characterization of growth and exopolysaccharide production of selected acetic acid bacteria in buckwheat sourdoughs. Int. J. Food Microbiol. 239 (2016), 103–112.
73. Villanueva, M., Mauro, R.R., Collar, C., Ronda, F., Acidification of protein-enriched rice starch doughs: effects on breadmaking. Eur. Food Res. Technol. 240 (2015), 783–794.
74. Vogel, R.F., Bocker, G., Stolz, P., Ehrmann, M., Fanta, D., Ludwig, W., Pot, B., Kersters, K., Schleifer, K.H., Hammes, W.P., Identification of lactobacilli from sourdough and description of Lactobacillus pontis sp. nov. Int. J. Syst. Bacteriol. 44 (1994), 223–229.
75. Vogelmann, S.A., Seitter, M., Singer, U., Brandt, M.J., Hertel, C., Adaptability of lactic acid bacteria and yeasts to sourdoughs prepared from cereals, pseudocereals and cassava and use of competitive strains as starters. Int. J. Food Microbiol. 130 (2009), 205–212.