1887

Abstract

is a lactic acid bacterium that characterizes the sourdough environment. The genetic differences of 24 strains isolated in different years from sourdoughs, mostly collected in Italy, were examined and compared by PFGE and multilocus sequence typing (MLST). The MLST scheme, based on the analysis of six housekeeping genes (, and ) was developed for this study. PFGE with the restriction enzyme I proved to have higher discriminatory power, since it revealed 22 different pulsotypes, while 19 sequence types were recognized through MLST analysis. Notably, restriction profiles generated from three isolates collected from the same firm but in three consecutive years clustered in a single pulsotype and showed the same sequence type, emphasizing the fact that the main factors affecting the dominance of a strain are correlated with processing conditions and the manufacturing environment rather than the geographical area. All results indicated a limited recombination among genes and the presence of a clonal population in The MLST scheme proposed in this work can be considered a useful tool for characterization of isolates and for in-depth examination of the strain diversity and evolution of this species.

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2010-07-01
2019-12-09
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References

  1. Arendt, E. K., Ryan, L. A. M. & Dal Bello, F. ( 2007; ). Impact of sourdough on the texture of bread. Food Microbiol 24, 165–174.[CrossRef]
    [Google Scholar]
  2. Bilhère, E., Lucas, P. M., Claisse, O. & Lonvaud-Funel, A. ( 2009; ). Multilocus sequence typing of Oenococcus oeni: detection of two subpopulations shaped by intergenic recombination. Appl Environ Microbiol 75, 1291–1300.[CrossRef]
    [Google Scholar]
  3. Borgo, F., Ricci, G., Manachini, P. L. & Fortina, M. G. ( 2007; ). Multilocus restriction typing: a tool for studying molecular diversity within Lactobacillus helveticus of dairy origin. Int Dairy J 17, 336–342.[CrossRef]
    [Google Scholar]
  4. Cai, H., Rodriguez, B. T., Zhang, W., Broadbent, J. R. & Steele, J. L. ( 2007; ). Genotypic and phenotypic characterization of Lactobacillus casei strains isolated from different ecological niches suggests frequent recombination and niche specificity. Microbiology 153, 2655–2665.[CrossRef]
    [Google Scholar]
  5. Catzeddu, P., Mura, E., Parente, E., Sanna, M. & 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.[CrossRef]
    [Google Scholar]
  6. Corsetti, A., Gobbetti, M., Balestrieri, F., Paoletti, F., Russi, L. & Rossi, J. ( 1998a; ). Sourdough lactic acid bacteria effects on bread firmness and staling. J Food Sci 63, 347–351.
    [Google Scholar]
  7. Corsetti, A., Gobbetti, M., Rossi, J. & Damiani, P. ( 1998b; ). Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Appl Microbiol Biotechnol 50, 253–256.[CrossRef]
    [Google Scholar]
  8. Corsetti, A., Gobbetti, M., De Marco, B., Balestrieri, F., Paoletti, F., Russi, L. & Rossi, J. ( 2000; ). Combined effects of sourdough lactic acid bacteria on bread firmness and staling. J Agric Food Chem 48, 3044–3051.[CrossRef]
    [Google Scholar]
  9. Corsetti, A., Lavermicocca, P., Morea, M., Baruzzi, F., Tosti, N. & Gobbetti, M. ( 2001; ). Phenotypic and molecular characterization 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, 95–104.[CrossRef]
    [Google Scholar]
  10. Corsetti, A., Settanni, L., Valmorri, S., Mastrangelo, M. & Suzzi, G. ( 2007; ). Identification of subdominant sourdough lactic acid bacteria and their evolution during laboratory-scale fermentations. Food Microbiol 24, 592–600.[CrossRef]
    [Google Scholar]
  11. De Angelis, M., Di Cagno, R., Gallo, G., Curci, M., Siragusa, S., Crecchio, C., Parente, E. & Gobbetti, M. ( 2007; ). Molecular and functional characterization of Lactobacillus sanfranciscensis strains isolated from sourdough. Int J Food Microbiol 114, 69–82.[CrossRef]
    [Google Scholar]
  12. De las Rivas, B., Marcobal, A. & Muñoz, R. ( 2004; ). Allelic diversity and population structure in Oenococcus oeni as determined from sequence analysis of housekeeping genes. Appl Environ Microbiol 70, 7210–7219.[CrossRef]
    [Google Scholar]
  13. De las Rivas, B., Marcobal, A. & Muñoz, R. ( 2006; ). Development of a multilocus sequence typing method for analysis of Lactobacillus plantarum strains. Microbiology 152, 85–93.[CrossRef]
    [Google Scholar]
  14. De Vuyst, L. & Neysens, P. ( 2005; ). The sourdough microflora: biodiversity and metabolic interactions. Trends Food Sci Technol 16, 43–56.[CrossRef]
    [Google Scholar]
  15. De Vuyst, L., Vrancken, G., Ravyts, F., Rimaux, T. & Weckx, S. ( 2009; ). Biodiversity, ecological determinants, and metabolic exploitation of sourdough microbiota. Food Microbiol 26, 666–675.[CrossRef]
    [Google Scholar]
  16. Diancourt, L., Passet, V., Chervaux, C., Garault, P., Smokvina, T. & Brisse, S. ( 2007; ). Multilocus sequence typing of Lactobacillus casei reveals a clonal population structure with low levels of homologous recombination. Appl Environ Microbiol 73, 6601–6611.[CrossRef]
    [Google Scholar]
  17. Di Cagno, R., De Angelis, M., Lavermicocca, P., De Vincenzi, M., Giovannini, C. & Gobbetti, M. ( 2002; ). Proteolysis by sourdough lactic acid bacteria: effects on wheat flour protein fractions and gliadin peptides involved in human cereal intolerance. Appl Environ Microbiol 68, 623–633.[CrossRef]
    [Google Scholar]
  18. Di Cagno, R., De Angelis, M., Auricchio, S., Greco, L., Clarke, C., De Vincenzi, M., Giovannini, C., D'Archivio, M., Landolfo, F. & other authors ( 2004; ). Sourdough bread made from wheat and nontoxic flours and started with selected lactobacilli is tolerated in celiac sprue patients. Appl Environ Microbiol 70, 1088–1096.[CrossRef]
    [Google Scholar]
  19. Di Cagno, R., De Angelis, M., Alfonsi, G., De Vincenzi, M., Silano, M., Vincentini, O. & Gobbetti, M. ( 2005; ). Pasta made from durum wheat semolina fermented with selected lactobacilli as a tool for a potential decrease of the gluten intolerance. J Agric Food Chem 53, 4393–4402.[CrossRef]
    [Google Scholar]
  20. Foschino, R., Arrigoni, C., Picozzi, C., Mora, D. & Galli, A. ( 2001; ). Phenotypic and genotypic aspects of Lactobacillus sanfranciscensis isolated from sourdoughs in Italy. Food Microbiol 18, 277–285.[CrossRef]
    [Google Scholar]
  21. Gobbetti, M., Corsetti, A. & Rossi, J. ( 1996; ). Lactobacillus sanfrancisco, a key sourdough lactic acid bacterium: physiology, genetic and biotechnology. Adv Food Sci 18, 167–175.
    [Google Scholar]
  22. Gobbetti, M., Rizzello, C. G., Di Cagno, R. & De Angelis, M. ( 2007; ). Sourdough lactobacilli and celiac disease. Food Microbiol 24, 187–196.[CrossRef]
    [Google Scholar]
  23. Hansen, A. & Schieberle, P. ( 2005; ). Generation of aroma compounds during sourdough fermentation: applied and fundamental aspects. Trends Food Sci Technol 16, 85–94.[CrossRef]
    [Google Scholar]
  24. Haubold, B. & Hudson, R. R. ( 2000; ). LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage analysis. Bioinformatics 16, 847–848.[CrossRef]
    [Google Scholar]
  25. Huson, D. H. & Bryant, D. ( 2006; ). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23, 254–267.
    [Google Scholar]
  26. Johnson, J. K., Arduino, S. M., Colin Stine, O., Johnson, J. & Harris, A. D. ( 2007; ). Multilocus sequence typing compared to pulsed-field gel electrophoresis for molecular typing of Pseudomonas aeruginosa. J Clin Microbiol 45, 3707–3712.[CrossRef]
    [Google Scholar]
  27. Korakli, M., Rossmann, A., Ganzle, M. G. & Vogel, R. F. ( 2001; ). Sucrose metabolism and exopolysaccharide production in wheat and rye sourdoughs by Lactobacillus sanfranciscensis. J Agric Food Chem 49, 5194–5200.[CrossRef]
    [Google Scholar]
  28. Korakli, M., Pavlovic, M., Ganzle, M. G. & Vogel, R. F. ( 2003; ). Exopolysaccharide and kestose production by Lactobacillus sanfranciscensis LTH2590. Appl Environ Microbiol 69, 2073–2079.[CrossRef]
    [Google Scholar]
  29. Kumar, S., Tamura, K. & Nei, M. ( 1994; ). mega: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput Appl Biosci 10, 189–191.
    [Google Scholar]
  30. Lacaze, G., Wick, M. & Cappelle, S. ( 2007; ). Emerging fermentation technologies: development of novel sourdough. Food Microbiol 24, 155–160.[CrossRef]
    [Google Scholar]
  31. Liljeberg, H. G. M. & Björck, I. M. E. ( 1996; ). Delayed gastric emptying rate as a potential mechanism for lowered glycemia after eating sourdough bread: studies in humans and rats using test products with added organic acids or an organic salt. Am J Clin Nutr 64, 886–893.
    [Google Scholar]
  32. Liljeberg, H. G. M., Lönner, C. H. & Björck, I. M. E. ( 1995; ). Sourdough fermentation or addition of organic acids or corresponding salts to bread improves nutritional properties of starch in healthy humans. J Nutr 125, 1503–1511.
    [Google Scholar]
  33. Meroth, C. B., Walter, J., Hertel, C., Brandt, M. J. & Hammes, W. P. ( 2003; ). Monitoring the bacterial population dynamics in sourdough fermentation processes by using PCR-denaturing gradient gel electrophoresis. Appl Environ Microbiol 69, 475–482.[CrossRef]
    [Google Scholar]
  34. Moore, M. M., Juga, B., Schober, T. J. & Arendt, E. K. ( 2007; ). Effect of lactic acid bacteria on properties of gluten-free sourdoughs, batters, and quality and ultrastructure of gluten-free bread. Cereal Chem 84, 357–364.[CrossRef]
    [Google Scholar]
  35. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
    [Google Scholar]
  36. Picozzi, C., Gallina, S., Della Fera, T. & Foschino, R. ( 2005; ). Comparison of cultural media for the enumeration of sourdough lactic acid bacteria. Ann Microbiol 55, 319–320.
    [Google Scholar]
  37. Picozzi, C., D'Anchise, F. & Foschino, R. ( 2006; ). PCR detection of Lactobacillus sanfranciscensis in sourdough and panettone baked product. Eur Food Res Technol 222, 330–335.[CrossRef]
    [Google Scholar]
  38. Picozzi, C., Vigentini, I. & Foschino, R. ( 2009; ). How long does the same strain of Lactobacillus sanfranciscensis inhabit a panettone sourdough? In 4th International Symposium on Sourdough – from Arts to Science, 14–17 October 2009, Freising, Germany, p. 28.
  39. Randazzo, C. L., Heilig, H., Restuccia, C., Giudici, P. & Caggia, C. ( 2005; ). Bacterial population in traditional sourdough evaluated by molecular methods. J Appl Microbiol 99, 251–258.[CrossRef]
    [Google Scholar]
  40. Ravelo, C., Magarinos, B., Lopez-Romalde, S., Toranzo, A. E. & Romalde, J. ( 2003; ). Molecular fingerprinting of fish-pathogenic Lactococcus garvieae strains by random amplified polymorphic DNA analysis. J Clin Microbiol 41, 751–756.[CrossRef]
    [Google Scholar]
  41. Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. ( 1998; ). Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci U S A 95, 6239–6244.[CrossRef]
    [Google Scholar]
  42. Scheirlinck, I., Van der Meulen, R., De Vuyst, L., Vandamme, P. & Huys, G. ( 2009; ). Molecular source tracking of predominant lactic acid bacteria in traditional Belgian sourdoughs and their production environments. J Appl Microbiol 106, 1081–1092.[CrossRef]
    [Google Scholar]
  43. Schnürer, J. & Magnusson, J. ( 2005; ). Antifungal lactic acid bacteria as biopreservatives. Trends Food Sci Technol 16, 70–78.[CrossRef]
    [Google Scholar]
  44. Smith, J. M., Smith, N. H., O'Rourke, M. & Spratt, B. G. ( 1993; ). How clonal are bacteria? Proc Natl Acad Sci U S A 90, 4384–4388.[CrossRef]
    [Google Scholar]
  45. Tanganurat, W., Quinquis, B., Leelawatcharamas, V. & Bolotin, A. ( 2009; ). Genotypic and phenotypic characterization of Lactobacillus plantarum strains isolated from Thai fermented fruits and vegetables. J Basic Microbiol 49, 377–385.[CrossRef]
    [Google Scholar]
  46. Tenover, F. C., Arbeit, R. D., Goering, R. V., Mickelsen, P. A., Murray, B. E., Persing, D. H. & Swaminathan, B. ( 1995; ). Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33, 2233–2239.
    [Google Scholar]
  47. Thiele, C., Ganzle, M. G. & Vogel, R. F. ( 2002; ). Contribution of sourdough lactobacilli, yeast, and cereal enzymes to the generation of amino acids in dough relevant for bread flavour. Cereal Chem 79, 45–51.[CrossRef]
    [Google Scholar]
  48. Tieking, M. & Gänzle, M. G. ( 2005; ). Exopolysaccharides from cereal-associated lactobacilli. Trends Food Sci Technol 16, 79–84.[CrossRef]
    [Google Scholar]
  49. Valcheva, R., Kabadjova, P., Racman, C., Ivanova, I., Onno, B., Prévost, H. & Dousset, X. ( 2007; ). A rapid PCR procedure for the specific identification of Lactobacillus sanfranciscensis, based on the 16S–23S intergenic spacer regions. J Appl Microbiol 102, 290–302.[CrossRef]
    [Google Scholar]
  50. Vogel, R. F., Muller, M., Stoltz, P. & Ehrmann, M. ( 1996; ). Ecology in sourdoughs produced by traditional and modern technology. Adv Food Sci 18, 152–159.
    [Google Scholar]
  51. Vogel, R. F., Knorr, R., Muller, M. R. A., Steudel, U., Ganzle, M. G. & Ehrmann, M. A. ( 1999; ). Non-dairy lactic fermentation: the cereal world. Antonie Van Leeuwenhoek 76, 403–411.[CrossRef]
    [Google Scholar]
  52. Vogel, R. F., Liebl, W., Rattei, T., Pavlovic, M. & Ehrmann, M. ( 2009; ). Lactobacillus sanfranciscensis – insights from the genome. In 4th International Symposium on Sourdough – from Arts to Science, 14–17 October 2009, Freising, Germany, p. 21.
  53. Zapparoli, G., Torriani, S. & Dellaglio, F. ( 1998; ). Differentiation of Lactobacillus sanfranciscensis strains by randomly amplified polymorphic DNA and pulsed-field gel electrophoresis. FEMS Microbiol Lett 166, 325–332.[CrossRef]
    [Google Scholar]
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