Identification and characterization of lactic acid bacteria and yeasts of PDO Tuscan bread sourdough by culture dependent and independent methods

International Journal of Food Microbiology

Volumn 250, Issue , 2017, Pages 19-26

  Palla, Michela ^a   Cristani, Caterina ^a   Giovannetti, Manuela ^a   Agnolucci, Monica ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

ARDRA; Candida milleri; ITS RFLP; Lactobacillus sanfranciscensis; PCR DGGE; Saccharomyces cerevisiae

Indexed keywords

AMPLIFIED RIBOSOMAL DNA RESTRICTION ANALYSIS; BACTERIUM ISOLATE; BREAD; CANDIDA; CONSERVATIONAL SEED BANK; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; FUNGAL CELL CULTURE; HUMAN; IDENTITY; LACTIC ACID BACTERIUM; LACTOBACILLUS; MICROFLORA; NONHUMAN; POLYMERASE CHAIN REACTION; RANDOMIZED CONTROLLED TRIAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SACCHAROMYCES CEREVISIAE; SPECIES COMPOSITION; CLASSIFICATION; DRIED YEAST; FERMENTATION; GENETICS; ISOLATION AND PURIFICATION; ITALY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR TYPING;

LACTIC ACID; RIBOSOMAL SPACER DNA; RIBOSOME DNA; RIBOSOME RNA; RNA, RIBOSOMAL, 26S;

BREAD; CANDIDA; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; FERMENTATION; ITALY; LACTIC ACID; LACTOBACILLUS; MICROBIOTA; MOLECULAR TYPING; MYCOLOGICAL TYPING TECHNIQUES; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; YEAST, DRIED;

EID: 85016250175     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2017.03.015     Document Type: Article

References (64)

1. Agnolucci, M., Cristani, C., Battini, F., Palla, M., Cardelli, R., Saviozzi, A., Nuti, M., Microbially-enhanced composting of olive mill solid waste (wet husk): bacterial and fungal community dynamics at industrial pilot and farm level. Bioresour. Technol. 134 (2013), 10–16.
2. Arendt, E.K., Ryan, L.A., Dal Bello, F., Impact of sourdough on the texture of bread. Food Microbiol. 24 (2007), 165–174.
3. Bae, H.D., Yanke, L.J., Cheng, K.J., Selinger, L.B., A novel staining method for detecting phytase activity. J. Microbiol. Methods 39 (1999), 17–22.
4. Catzeddu, P., Mura, E., Parente, E., Sanna, M., Farris, G.A., Molecular characterization of lactic acid bacteria from sourdough breads produced in Sardinia (Italy) and multivariate statistical analyses of results. Syst. Appl. Microbiol. 29 (2006), 138–144.
5. Cocolin, L., Bisson, L.F., Mills, D.A., Direct profiling of the yeast dynamics in wine fermentations. FEMS Microbiol. Lett. 189 (2000), 81–87.
6. Cocolin, L., Alessandria, V., Dolci, P., Gorra, R., Rantsiou, K., Culture independent methods to assess the diversity and dynamics of microbiota during food fermentations. Int. J. Food Microbiol. 167 (2013), 29–43.
7. Corsetti, A., Technology of sourdough fermentation and sourdough applications. Gobbetti, M., Gänzle, M., (eds.) Handbook on Sourdough Biotechnology, 2013, Springer, New York, 85–104.
8. Corsetti, A., Lavermicocca, P., Morea, M., Baruzzi, F., Tosti, N., Gobbetti, M., Phenotypic and molecular identification and clustering of lactic acid bacteria and yeasts from wheat (species Triticum durum and Triticum aestivum) sourdoughs of southern Italy. Int. J. Food Microbiol. 64 (2001), 95–104.
9. De Man, J.C., Rogosa, D., Sharpe, M.E., A medium for the cultivation of lactobacilli. J. Appl. Microbiol. 23 (1960), 130–135.
10. De Vuyst, L., Neysens, P., The sourdough microflora: biodiversity and metabolic interactions. Trends Food Sci. Technol. 16 (2005), 43–56.
11. 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. 37 (2014), 11–29.
12. De Vuyst, L., Harth, H., Van Kerrebroeck, S., Leroy, F., Yeast diversity of sourdoughs and associated metabolic properties and functionalities. Int. J. Food Microbiol. 239 (2016), 26–34.
13. Dertli, E., Mercan, E., Arıcı, M., Yılmaz, M.T., Sağdıç, O., Characterisation of lactic acid bacteria from Turkish sourdough and determination of their exopolysaccharide (EPS) production characteristics. LWT Food Sci. Technol. 71 (2016), 116–124.
14. Edgar, R.C., MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinf., 5, 2004, 1.
15. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004), 1792–1797.
16. Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985), 783–791.
17. Ferchichi, M., Valcheva, R., Oheix, N., Kabadjova, P., Prévost, H., Onno, B., Dousset, X., Rapid investigation of French sourdough microbiota by restriction fragment length polymorphism of the 16S-23S rRNA gene intergenic spacer region. World J. Microbiol. Biotechnol. 24 (2008), 2425–2434.
18. Fernández-Espinar, M.T., Esteve-Zarzoso, B., Querol, A., Barrio, E., RFLP analysis of the ribosomal internal transcribed spacers and the 5.8S rRNA gene region of the genus Saccharomyces: a fast method for species identification and the differentiation of flor yeasts. Antonie Van Leeuwenhoek 78 (2000), 87–97.
19. Foschino, R., Arrigoni, C., Mora, D., Galli, A., Phenotypic and genotypic aspects of Lactobacillus sanfranciscensis strains isolated from sourdoughs in Italy. Food Microbiol. 18 (2001), 277–285.
20. Gänzle, M., Ripari, V., Composition and function of sourdough microbiota: From ecological theory to bread quality. Int. J. Food Microbiol. 239 (2016), 19–25.
21. Gatto, V., Torriani, S., Microbial population changes during sourdough fermentation monitored by DGGE analysis of 16S and 26S rRNA gene fragments. Ann. Microbiol. 54 (2004), 31–42.
22. Gobbetti, M., The sourdough microflora: interactions of lactic acid bacteria and yeasts. Trends Food Sci. Technol. 9 (1998), 267–274.
23. Gobbetti, M., Gänzle, M., Handbook on Sourdough Biotechnology. first ed., 2013, Springer, New York.
24. 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.
25. Gullo, M., Romano, A.D., Pulvirenti, A., Giudici, P., Candida humilis - dominant species in sourdoughs for the production of durum wheat bran flour bread. Int. J. Food Microbiol. 80 (2003), 55–59.
26. Iacumin, L., Cecchini, F., Manzano, M., Osualdini, M., Boscolo, D., Orlic, S., Comi, G., Description of the microflora of sourdoughs by culture-dependent and culture-independent methods. Food Microbiol. 26 (2009), 128–135.
27. Istituto Nazionale di Sociologia Rurale, Atlante dei prodotti tipici: il pane. 2000, Agra-Rai Eri, Rome, Italy, 13.
28. Jacques, N., Sarilar, V., Urien, C., Lopes, M.R., Morais, C.G., Uetanabaro, A.P.T., Tinsley, C.R., Rosa, C.A., Sicard, D., Casaregola, S., Three novel ascomycetous yeast species of the Kazachstania clade, Kazachstania saulgeensis sp. nov., Kazachstania serrabonitensis sp. nov. and Kazachstania australis sp. nov. Reassignement of Candida humilis to Kazachastania humilis fa comb nov and Candida pseudohumilis to Kazachstania pseudohumilis fa comb. nov. Int. J. Syst. Evol. Microbiol. 66 (2016), 5192–5200.
29. Jorquera, M.A., Hernández, M.T., Rengel, Z., Marschner, P., de la Luz Mora, M., Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil. Biol. Fertil. Soils 44 (2008), 1025–1034.
30. Katina, K., Arendt, E., Liukkonen, K.H., Autio, K., Flander, L., Poutanen, K., Potential of sourdough for healthier cereal products. Trends Food Sci. Technol. 16 (2005), 104–112.
31. Kimura, M., A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 (1980), 111–120.
32. Kline, L., Sugihara, T.F., Microorganisms of the San Francisco sour dough bread process II. Isolation and characterization of undescribed bacterial species responsible for the souring activity. Appl. Microbiol. 21 (1971), 459–465.
33. Kurtzman, C.P., Robnett, C.J., Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73 (1998), 331–371.
34. Kurtzman, C.P., Robnett, C.J., Phylogenetic relationships among yeasts of the ‘Saccharomyces Complex’ determined from multigene sequence analyses. FEMS Yeast Res. 3 (2003), 417–432.
35. Lachance, M.A., Boekhout, T., Scorzetti, G., Fell, J.W., Kurtzman, C.P., Candida Berkhout. Kurtzman, C., Fell, J.W., Boekhout, T., (eds.) The Yeasts: A Taxonomic Study, fifth ed., vol. 2, 2011, Elsevier, Amsterdam (NL), 987–1278.
36. Lane, D.J., 16S/23S rRNA sequencing. Stackebrandt, E., Goodfellow, M., (eds.) Nucleic Acid Techniques in Bacterial Systematics, 1991, Wiley, New York, 115–175.
37. Lattanzi, A., Minervini, F., Di Cagno, R., Diviccaro, A., Antonielli, L., Cardinali, G., Cappelle, S., De Angelis, M., Gobbetti, M., The lactic acid bacteria and yeast microbiota of eighteen sourdoughs used for the manufacture of traditional Italian sweet leavened baked goods. Int. J. Food Microbiol. 163 (2013), 71–79.
38. Liu, T., Li, Y., Chen, J., Sadiq, F.A., Zhang, G., Li, Y., He, G., Prevalence and diversity of lactic acid bacteria in Chinese traditional sourdough revealed by culture dependent and pyrosequencing approaches. LWT Food Sci. Technol. 68 (2016), 91–97.
39. Minervini, F., Di Cagno, R., Lattanzi, A., De Angelis, M., Antonielli, L., Cardinali, G., Cappelle, S., Gobbetti, M., Lactic acid bacterium and yeast microbiotas of 19 sourdoughs used for traditional/typical Italian breads: interactions between ingredients and microbial species diversity. Appl. Environ. Microbiol. 78 (2012), 1251–1264.
40. Minervini, F., De Angelis, M., Di Cagno, R., Gobbetti, M., Ecological parameters influencing microbial diversity and stability of traditional sourdough. Int. J. Food Microbiol. 171 (2014), 136–146.
41. Nuobariene, L., Hansen, Å.S., Arneborg, N., Isolation and identification of phytase-active yeasts from sourdoughs. LWT Food Sci. Technol. 48 (2012), 190–196.
42. Osimani, A., Zannini, E., Aquilanti, L., Mannazzu, I.M., Comitini, F., Clementi, F., Lactic acid bacteria and yeasts from wheat sourdoughs of the Marche region. Ital. J. Food Sci. 21 (2009), 269–286.
43. Palla, M., Cristani, C., Giovannetti, M., Agnolucci, M., Identificazione molecolare di batteri lattici e lieviti caratterizzanti l'impasto acido per la produzione di Pane Toscano a lievitazione naturale. Ind. Aliment. 54 (2015), 5–11.
44. Palomba, S., Blaiotta, G., Ventorino, V., Saccone, A., Pepe, O., Microbial characterization of sourdough for sweet baked products in the Campania region (southern Italy) by a polyphasic approach. Ann. Microbiol. 61 (2011), 307–314.
45. Pulvirenti, A., Caggia, C., Restuccia, C., Gullo, M., Giudici, P., DNA fingerprinting methods used for identification of yeasts isolated from Sicilian sourdoughs. Ann. Microbiol. 51 (2001), 107–120.
46. Randazzo, C.L., Heilig, H., Restuccia, C., Giudici, P., Caggia, C., Bacterial population in traditional sourdough evaluated by molecular methods. J. Appl. Microbiol. 99 (2005), 251–258.
47. Reale, A., Tremonte, P., Succi, M., Sorrentino, E., Coppola, R., Exploration of lactic acid bacteria ecosystem of sourdoughs from the Molise region. Ann. Microbiol. 55 (2005), 17–22.
48. Ricciardi, A., Parente, E., Piraino, P., Paraggio, M., Romano, P., Phenotypic characterization of lactic acid bacteria from sourdoughs for Altamura bread produced in Apulia (Southern Italy). Int. J. Food Microbiol. 98 (2005), 63–72.
49. Saitou, N., Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987), 406–425.
50. Scheirlinck, I., Van der Meulen, R., Van Schoor, A., Vancanneyt, M., De Vuyst, L., Vandamme, P., Huys, G., Influence of geographical origin and flour type on diversity of lactic acid bacteria in traditional Belgian sourdoughs. Appl. Environ. Microbiol. 73 (2007), 6262–6269.
51. Settanni, L., Valmorri, S., van Sinderen, D., Suzzi, G., Paparella, A., Corsetti, A., Combination of multiplex PCR and PCR-denaturing gradient gel electrophoresis for monitoring common sourdough-associated Lactobacillus species. Appl. Environ. Microbiol. 72 (2006), 3793–3796.
52. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30 (2013), 2725–2729.
53. Valmorri, S., Settanni, L., Suzzi, G., Gardini, F., Vernocchi, P., Corsetti, A., Application of a novel polyphasic approach to study the lactobacilli composition of sourdoughs from the Abruzzo region (central Italy). Lett. Appl. Microbiol. 43 (2006), 343–349.
54. Valmorri, S., Tofalo, R., Settanni, L., Corsetti, A., Suzzi, G., Yeast microbiota associated with spontaneous sourdough fermentations in the production of traditional wheat sourdough breads of the Abruzzo region (Italy). Antonie Van Leeuwenhoek 97 (2010), 119–129.
55. Venturi, M., Guerrini, S., Vincenzini, M., Stable and non-competitive association of Saccharomyces cerevisiae, Candida milleri and Lactobacillus sanfranciscensis during manufacture of two traditional sourdough baked goods. Food Microbiol. 31 (2012), 107–115.
56. Vera, A., Ly-Chatain, M.H., Rigobello, V., Demarigny, Y., Description of a French natural wheat sourdough over 10 consecutive days focussing on the lactobacilli present in the microbiota. Antonie Van Leeuwenhoek 101 (2012), 369–377.
57. Vernocchi, P., Valmorri, S., Gatto, V., Torriani, S., Gianotti, A., Suzzi, G., Guerzoni, M.E., Gardini, F., A survey on yeast microbiota associated with an Italian traditional sweet-leavened baked good fermentation. Food Res. Int. 37 (2004), 469–476.
58. Vigentini, I., Antoniani, D., Roscini, L., Comasio, A., Galafassi, S., Picozzi, C., Corte, L., Compagno, C., Dal Bello, F., Cardinali, G., Foschino, R., Candida milleri species reveals intraspecific genetic and metabolic polymorphisms. Food Microbiol. 42 (2014), 72–81.
59. Walter, J., Hertel, C., Tannock, G.W., Lis, C.M., Munro, K., Hammes, W.P., Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67 (2001), 2578–2585.
60. Weisburg, W.G., Barns, S.M., Pelletier, D.A., Lane, D.J., 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173 (1991), 697–703.
61. White, T.J., Bruns, T., Lee, S., Taylor, J.W., Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., (eds.) PCR Protocols: A Guide to Methods and Applications, 1990, Academic Press Inc., New York, 315–322.
62. Yazar, G., Tavman, Ş., Functional and technological aspects of sourdough fermentation with Lactobacillus sanfranciscensis. Food Eng. Rev. 4 (2012), 171–190.
63. Zhang, J., Liu, W., Sun, Z., Bao, Q., Wang, F., Yu, J., Chen, W., Zhang, H., Diversity of lactic acid bacteria and yeasts in traditional sourdoughs collected from western region in Inner Mongolia of China. Food Control 22 (2011), 767–774.
64. Zotta, T., Piraino, P., Parente, E., Salzano, G., Ricciardi, A., Characterization of lactic acid bacteria isolated from sourdoughs for Cornetto, a traditional bread produced in Basilicata (Southern Italy). World J. Microbiol. Biotechnol. 24 (2008), 1785–1795.