Different flour microbial communities drive to sourdoughs characterized by diverse bacterial strains and free amino acid profiles

Frontiers in Microbiology

Volumn 7, Issue NOV, 2016, Pages

  Celano, Giuseppe ^a   De Angelis, Maria ^a   Minervini, Fabio ^a   Gobbetti, Marco ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Bacterial strains; Enterobacteria; Free amino acids; Irradiated flour; Lactic acid bacteria; Sourdough; Yeasts

Indexed keywords

ALCOHOL; AMINO ACID; AMYLASE; ASPARTIC ACID; CARBOHYDRATE; CARBOXYLIC ACID; ISOLEUCINE; LEUCINE; RIBOSOME RNA; RNA 16S; RNA 26S; THREONINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; CELL DENSITY; CONTROLLED STUDY; DOUGH; ENTEROBACTERIACEAE; ESCHERICHIA; FIRMICUTES; FLOUR; GAMMA RADIATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LACTIC ACID BACTERIUM; LACTOBACILLUS CURVATUS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PANTOEA AGGLOMERANS; PEDIOCOCCUS PENTOSACEUS; POLYMERASE CHAIN REACTION; RANDOM AMPLIFIED POLYMORPHIC DNA; RNA GENE; SACCHAROMYCES CEREVISIAE; SOURDOUGH; WHEAT FLOUR; YEAST;

EID: 85006725015     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01770     Document Type: Article

References (67)

1. AACC international (2000). Approved Methods of Analysis. St. Paul, MN: AACC International.
2. Ahmed, W., Sawant, S., Huygens, F., Goonetilleke, A., and Gardner, T. (2009). Prevalence and occurrence of zoonotic bacterial pathogens in surface waters determined by quantitative PCR. Water Res. 43, 4918-4928. doi: 10.1016/j.watres.2009.03.041.
3. Alfonzo, A., Ventimiglia, G., Corona, O., Di Gerlando, R., Gaglio, R., Francesca, N., et al. (2013). Diversity and technological potential of lactic acid bacteria of wheat flours. Food Microbiol. 36, 343-354. doi: 10.1016/j.fm.2013.07.003.
4. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
5. Andreotti, R., Pérez de León, A. A., Dowd, S. E., Guerrero, F. D., Bendele, K. G., and Scoles, G. A. (2011). Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol. 11:6. doi: 10.1186/1471-2180-11-6.
6. Aslam, Z., Im, W. T., Ten, L. N., Lee, M. J., Kim, K. H., and Lee, S. T. (2006). Lactobacillus siliginis sp. nov., isolated from wheat sourdough in South Korea. Int. J. Syst. Evol. Microbiol. 56, 2209-2213. doi: 10.1099/ijs.0.64321-0.
7. Aziz, N. H., Souzan, R. M., and Shahin Azza, A. (2006). Effect of ?-irradiation on the occurrence of pathogenic microorganisms and nutritive value of four principal cereal grains. Appl. Radiat. Isot. 64, 1555-1562. doi: 10.1016/j.apradiso.2005.10.006.
8. Candogan, K., Wardlaw, F. B., and Acton, J. C. (2009). Effect of starter culture on proteolytic changes during processing of fermented beef sausages. Food Chem. 116, 731-737. doi: 10.1016/j.foodchem.2009.03.065.
9. Catzeddu, P. (2011). "Sourdough breads", in Flour and Breads and their Fortification in Health and Disease Prevention, eds V. Preedy, R. R. Watson, and V. B. Patel (London: Academic press), 37-46.
10. Catzeddu, P., Mura, E., Parente, E., Sanna, M., and Farris, G. A. (2006). Molecular characterization of lactic acid bacteria from sourdough breads produced in Sardinia (Italy) and multivariate statistical analyses of results. Syst. Appl. Microbiol. 29, 138-144. doi: 10.1016/j.syapm.2005.07.013.
11. Chao, A., and Bunge, J. (2002). Estimating the number of species in a stochastic abundance model. Biometrics 58, 531-539. doi: 10.1111/j.0006-341X.2002.00531.x.
12. Chen, Q., Liu, Q., Sun, Q., Kong, B., and Xiong, Y. (2015). Flavour formation from hydrolysis of pork sarcoplasmic protein extract by a unique LAB culture isolated from Harbin dry sausage. Meat Sci. 100, 110-117. doi: 10.1016/j.meatsci.2014.10.001.
13. Collar, C. (1996). Biochemical and technological assessment of the metabolism of pure and mixed cultures of yeast and lactic acid bacteria in breadmaking applications. Food Sci. Technol. Int. 2, 349-367. doi: 10.1177/108201329600200601.
14. Corsetti, A., Settanni, L., Valmorri, S., Mastrangelo, M., and Suzzi, G. (2007). Identification of subdominant sourdough lactic acid bacteria and their evolution during laboratory-scale fermentations. Food Microbiol. 24, 592-600. doi: 10.1016/j.fm.2007.01.002.
15. Corsetti, A., Settanni, L., and Van Sinderen, D. (2004). Characterization of bacteriocin-like inhibitory substances (BLIS) from sourdough lactic acid bacteria and evaluation of their in vitro and in situ activity. J. Appl. Microbiol. 96, 521-534. doi: 10.1111/j.1365-2672.2004.02171.x.
16. De Angelis, M., Corsetti, A., Tosti, N., Rossi, J., Corbo, M. R., and Gobbetti, M. (2001). Characterization of non-starter lactic acid bacteria from Italian ewe cheeses based on phenotypic, genotypic, and cell wall protein analyses. Appl. Environ. Microbiol. 67, 2011-2020. doi: 10.1128/AEM.67.5.2011-2020.2001.
17. De Angelis, M., Di Cagno, R., Gallo, G., Curci, M., Siragusa, S., Crecchio, C., et al. (2007). Molecular and functional characterization of Lactobacillus sanfranciscensis strains isolated from sourdoughs. Int. J. Food Microbiol. 114, 69-82. doi: 10.1016/j.ijfoodmicro.2006.10.036.
18. Del Bove, M., Lattanzi, M., Rellini, P., Pelliccia, C., Fatichenti, F., and Cardinali, G. (2009). Comparison of molecular and metabolomic methods as characterization tools of Debaryomyces hansenii cheese isolates. Food Microbiol. 26, 453-459. doi: 10.1016/j.fm.2009.03.009.
19. De Vuyst, L., Van Kerrebroeck, S., Harth, H., Huys, G., Daniel, H. M., and Weckx, S. (2014). Microbial ecology of sourdough fermentations: diverse or uniform? Food Microbiol. 37, 11-29. doi: 10.1016/j.fm.2013.06.002.
20. De Vuyst, L., Vrancken, G., Ravyts, F., Rimaux, T., and Weckx, S. (2009). Biodiversity, ecological determinants, and metabolic exploitation of sourdough microbiota. Food Microbiol. 26, 666-675. doi: 10.1016/j.fm.2009.07.012.
21. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461.
22. Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996-998. doi: 10.1038/nmeth.2604.
23. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381.
24. Ercolini, D., Pontonio, E., De Filippis, F., Minervini, F., La Storia, A., Gobbetti, M., et al. (2013). Microbial ecology dynamics during rye and wheat sourdough preparation. Appl. Environ. Microbiol. 79, 7827-7836. doi: 10.1128/AEM.02955-13.
25. Fadda, S., López, C., and Vignolo, G. (2010). Role of lactic acid bacteria during meat conditioning and fermentation: peptides generated as sensorial and hygienic biomarkers. Meat Sci. 86, 66-79. doi: 10.1016/j.meatsci.2010.04.023.
26. Fadda, S., Sanz, Y., Vignolo, G., Aristoy, M.-C., Oliver, G., and Toldrá, F. (1999). Hydrolysis of pork muscle sarcoplasmic proteins by Lactobacillus curvatus and Lactobacillus sakei. Appl. Environ. Microbiol. 65, 578-584.
27. Francés, R., Benlloch, S., Zapater, P., González, J. M., Lozano, B., Muñoz, C., et al. (2004). A sequential study of serum bacterial DNA in patients with advanced cirrhosis and ascites. Hepatology 39, 484-491. doi: 10.1002/hep.20055.
28. Gänzle, M. G., and Gobbetti, M. (2013). "Physiology and biochemistry of sourdough lactic acid bacteria", in Handbook of Sourdough Biotechnology, eds M. Gobbetti, and M. G. Gänzle (New York, NY: Springer Science + Business Media), 183-216.
29. Gobbetti, M., Corsetti, A., and Rossi, J. (1994). The sourdough microflora. Interactions between lactic acid bacteria and yeasts: metabolism of amino acids. World J. Microbiol. Biotechnol. 10, 275-279. doi: 10.1007/BF00414862.
30. Gobbetti, M., Rizzello, C. G., Di Cagno, R., and De Angelis, M. (2014). How the sourdough may affect the functional features of leavened baked goods. Food Microbiol. 37, 30-40. doi: 10.1016/j.fm.2013.04.012.
31. Gowen, C. M., and Fong, S. S. (2010). Genome-scale metabolic model integrated with RNAseq data to identify metabolic states of Clostridium thermocellum. Biotechnol. J. 7, 759-767. doi: 10.1002/biot.201000084.
32. Gu, C. T., Li, C. Y., Yang, L. J., and Huo, G. C. (2014). Enterobacter xiangfangensis sp. nov., isolated from Chinese traditional sourdough, and reclassification of Enterobacter sacchari Zhu et al. 2013 as Kosakonia sacchari comb. nov. Int. J. Syst. Evol. Microbiol. 64, 2650-2656. doi: 10.1099/ijs.0.064709-0.
33. Hammes, W. P., Brandt, M. J., Francis, K. L., Rosenheim, J., Seitter, M. F. H., and Vogelmann, S. A. (2005). Microbial ecology of cereal fermentations. Trends Food Sci. Technol. 16, 4-11. doi: 10.1016/j.tifs.2004.02.010.
34. Hammes, W. P., and Gänzle, M. G. (1997). "Sourdough breads and related products", in Microbiology of Fermented Foods Vol. 1, ed B. B. Wood (London: Blackie Academic and Professional), 199-216.
35. Handl, S., Dowd, S. E., Garcia-Mazcorro, J. F., Steiner, J. M., and Suchodolski, J. S. (2011). Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol. Ecol. 76, 301-310. doi: 10.1111/j.1574-6941.2011.01058.x.
36. Hanis, T., Mnukova, J., Jelen, P., Klir, P., Perez, B., and Pesek, M. (1988). Effect of gamma irradiation on survival of natural microflora and some nutrients in cereal meals. Cereal Chem. 65, 381-383.
37. Ito, H., and Yusop Abu, M. (1985). Study of microflora in Malaysian dried fishes and their decontamination by gamma-irradiation. Agric. Biol. Chem. 49, 1047-1051. doi: 10.1080/00021369.1985.10866861.
38. Kitahara, M., Sakaka, S., and Benno, Y. (2005). Biodiversity of Lactobacillus sanfranciscensis strains isolated from five sourdoughs. Lett. Appl. Microbiol. 40, 353-357. doi: 10.1111/j.1472-765X.2005.01678.x.
39. Kurtzman, C. P., and Robnett, C. J. (1998). Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73, 331-371.
40. Lattanzi, A., Minervini, F., Di Cagno, R., Diviccaro, A., Antonielli, L., Cardinali, G., et al. (2013). 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, 71-79. doi: 10.1016/j.ijfoodmicro.2013.02.010.
41. Lattanzi, A., Minervini, F., and Gobbetti, M. (2014). Assessment of comparative methods for storing type-I wheat sourdough. LWT Food Sci. Technol. 59, 948-955. doi: 10.1016/j.lwt.2014.06.032.
42. López, C. M., Sentandreu, M. A., Vignolo, G. M., and Fadda, S. G. (2015). Proteomic and peptidomic insights on myofibrillar protein hydrolysis in a sausage model during fermentation with autochthonous starter cultures. Food Res. Int. 78, 41-49. doi: 10.1016/j.foodres.2015.11.009.
43. Mihhalevski, A., Sarand, I., Viiard, E., Salumets, A., and Paalme, T. (2011). Growth characterization of individual rye sourdough bacteria by isothermal microcalorimetry. J. Appl. Microbiol. 110, 529-540. doi: 10.1111/j.1365-2672.2010.04904.x.
44. Minervini, F., Celano, G., Lattanzi, A., De Angelis, M., and Gobbetti, M. (2016). Added ingredients affect the microbiota and biochemical characteristics of durum wheat type-I sourdough. Food Microbiol. 60, 112-123. doi: 10.1016/j.fm.2016.05.016.
45. Minervini, F., De Angelis, M., Di Cagno, R., and Gobbetti, M. (2014). Ecological parameters influencing microbial diversity and stability of traditional sourdough. Int. J. Food Microbiol. 171, 136-146. doi: 10.1016/j.ijfoodmicro.2013.11.021.
46. Minervini, F., De Angelis, M., Di Cagno, R., Pinto, D., Siragusa, S., Rizzello, C. G., et al. (2010). Robustness of Lactobacillus plantarum starters during daily propagation of wheat flour sourdough type I. Food Microbiol. 27, 897-908. doi: 10.1016/j.fm.2010.05.021.
47. Minervini, F., Di Cagno, R., Lattanzi, A., De Angelis, M., Antonielli, L., Cardinali, G., et al. (2012b). 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, 1251-1264. doi: 10.1128/AEM.07721-11.
48. Minervini, F., Lattanzi, A., De Angelis, M., Celano, G., and Gobbetti, M. (2015). House microbiotas as sources of lactic acid bacteria and yeasts in traditional Italian sourdoughs. Food Microbiol. 52, 66-76. doi: 10.1016/j.fm.2015.06.009.
49. Minervini, F., Lattanzi, A., De Angelis, M., Di Cagno, R., and Gobbetti, M. (2012a). Influence of artisan bakery-or laboratory-propagated sourdoughs on the diversity of lactic acid bacterium and yeast microbiotas. Appl. Environ. Microbiol. 78, 5328-5340. doi: 10.1128/AEM.00572-12.
50. Onno, B., and Roussel, P. (1994). "Technologie et microbiologie de la panification au levain", in De Bactéries Lactiques, Aspects Fondamentaux et Technologiques Vol. 2, eds H. Roissart, and F. M. Luquet (Uriage, France), 293-321.
51. Ordóñez, J. A., Hierro, E. M., Bruna, J. M., and de la Hoz, L. (1999). Changes in the components of dry-fermented sausages during ripening. Crit. Rev. Food Sci. Nutr. 39, 329-367. doi: 10.1080/10408699991279204.
52. Paredi, G., Sentandreu, M.-A., Mozzarelli, A., Fadda, S., Hollung, K., and de Almeida, A. M. (2013). Muscle and meat: new horizons and applications for proteomics on a farm to fork perspective. J. Proteomics 88, 52-82. doi: 10.1016/j.jprot.2013.01.029.
53. Robert, H., Gabriel, V., and Fontagné-Faucher, C. (2009). Biodiversity of lactic acid bacteria in French wheat sourdough as determined by molecular characterization using species-specific PCR. Int. J. Food Microbiol. 135, 53-59. doi: 10.1016/j.ijfoodmicro.2009.07.006.
54. Scheirlinck, I., Van der Meulen, R., Van Schoor, A., Vancanneyt, M., De Vuyst, L., Vandamme, P., et al. (2007). Influence of the geographical origin and flour type on diversity of lactic acid bacteria in traditional Belgian sourdoughs. Appl. Environ. Microbiol. 73, 6262-6269. doi: 10.1128/AEM.00894-07.
55. Scheirlinck, I., Van Der Meulen, R., Van Schoor, A., Vancanneyt, M., De Vuyst, L., Vandamme, P., et al. (2008). Taxonomic structure and stability of the bacterial community in Belgian sourdough ecosystems as assessed by culture and population fingerprinting. Appl. Environ. Microbiol. 74, 2414-2423. doi: 10.1128/AEM.02771-07.
56. Shannon, C. E., and Weaver, W. (1949). The Mathematical Theory of Communication. Urbana, IL: University of Illinois Press.
57. Siragusa, S., Di Cagno, R., Ercolini, D., Minervini, F., Gobbetti, M., and De Angelis, M. (2009). Taxonomic structure and monitoring of the dominant population of lactic acid bacteria during wheat flour sourdough type I propagation using Lactobacillus sanfranciscensis starters. Appl. Environ. Microbiol. 75, 1099-1109. doi: 10.1128/AEM.01524-08.
58. Soteropoulos, P., and Perlin, D. S. (1998). Genetic probing of the stalk segments associated with M2 and M3 of the plasma membrane H+-ATPase from Saccharomyces cerevisiae. J. Biol. Chem. 273, 26426-26431. doi: 10.1074/jbc.273.41.26426.
59. Suchodolski, J. S., Dowd, S. E., Wilke, V., Steiner, J. M., and Jergens, A. E. (2012). 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease. PLoS ONE 7:e39333. doi: 10.1371/journal.pone.0039333.
60. Research Testing Laboratory (2016). Data from: Triticum turgidum subsp., durum Targeted Locus (Loci). NCBI Bioproject Database. Available online at: http://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA318402.
61. Van der Meulen, R., Scheirlinck, I., Van Schoor, A., Huys, G., Vancanneyt, M., Vandamme, P., et al. (2007). Population dynamics and metabolite target analysis during laboratory fermentations of wheat and spelt sourdoughs. Appl. Environ. Microbiol. 73, 4741-4750. doi: 10.1128/AEM.00315-07.
62. Velasco, R., Ordóñez, J. A., Cabeza, M. C., de la Hoz, L., and Cambero, M. I. (2011). Use of the E-beam radiation to diminish the late blowing of cheese. Int. Dairy J. 21, 493-500. doi: 10.1016/j.idairyj.2011.01.011.
63. Vogelmann, S. A., Seitter, M., Singer, U., Brandt, M. J., and Hertel, C. (2009). 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, 205-212. doi: 10.1016/j.ijfoodmicro.2009.01.020.
64. Weckx, S., Van der Meulen, R., Maes, D., Scheirlinck, I., Huys, G., Vandamme, P., et al. (2010). Lactic acid bacteria community dynamics and metabolite production of rye sourdough fermentations share characteristics of wheat and spelt sourdough fermentations. Food Microbiol. 27, 1000-1008. doi: 10.1016/j.fm.2010.06.005.
65. Zeppa, G., Conterno, L., and Gerbi, V. (2001). Determination of organic acids, sugars, diacetyl, and acetoin in cheese by high-performance liquid chromatography. J. Agric. Food Chem. 49, 2722-2726. doi: 10.1021/jf0009403.
66. Zhang, J., Kobert, K., Flouri, T., and Stamatakis, A. (2014). PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614-620. doi: 10.1093/bioinformatics/btt593.
67. Zotta, T., Piraino, P., Parente, E., Salzano, G., and Ricciardi, A. (2008). Characterization of lactic acid bacteria isolated from sourdoughs for Cornetto, a traditional bread produced in Basilicata (Southern Italy). World J. Microbiol. Biotechnol. 24, 1785-1795. doi: 10.1007/s11274-008-9671-0.