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Evidence for the presence of restriction/modification systems in Lactobacillus delbrueckii

  • Viviana Suárez (a1), Miriam Zago (a2), Giorgio Giraffa (a2), Jorge Reinheimer (a1) and Andrea Quiberoni (a1)...


The bacteriophages Cb1/204 and Cb1/342 were obtained by induction from the commercial strain Lactobacillus delbrueckii subsp. lactis Cb1, and propagated on Lactobacillus delbrueckii subsp. lactis 204 (Lb.l 204) and Lactobacillus delbrueckii subsp. bulgaricus 342 (Lb.b 342), respectively. By cross sensitivity, it was possible to detect a delay in the lysis of Lb.l 204 with Cb1/342 phage, while the adsorption rate was high (99·5%). Modified and unmodified phages were isolated using phage Cb1/342 and strain Lb.l 204. The EOP (Efficiency of Plaquing) values for the four phages (Cb1/204, Cb1/342, Cb1/342modified and Cb1/342unmodified) suggested that an R/M system modified the original temperate phage, and the BglII-DNA restriction patterns of these phages might point out the presence of a Type II R/M system. Also, the existence of a Type I R/M system was demonstrated by PCR and nucleotide sequence, being the percentages of alignment homology with Type I R/M systems reported previously higher than 95%. In this study it was possible to demonstrate that the native phage resistant mechanisms and the occurrence of prophages in commercial host strains, contribute strongly to diversify the phage population in a factory environment.


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Allison, G & Klaenhammer, T 1998 Phage resistance mechanisms in lactic acid bacteria. International Dairy Journal 8 207226
Auad, L, Ascárate, Peril A, Ruiz Holgado, A & Raya, R 1998 Evidence of a restriction/modification system in Lactobacillus delbrueckii subsp. lactis CNRZ 326. Current Microbiology 36 271273
Barrangou, R, Fremaux, C, Deveau, H, Richards, M, Boyaval, P, Moineau, S, Romero, DA & Horvath, P 2007 CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes. Science 315 17091712
Bourniquel, A 2000 Molecuar insights into the metabolism and physiology of the lactic acid bacterium Lactobacillus delbrueckii subsp. lactis. Thesis Department of Molecular Microbiology Biozentrum der Universitaet Basel Basel, Switzerland
Bourniquel, A, Casey, M, Mollet, B & Pridmore, D 2002 DNA sequence and functional analysis of Lactobacillus delbrueckii subsp. lactis plasmids pN42 and pJBL2. Plasmid 47 153157
Candioti, MC, Hynes, ER, Perotti, MC & Zalazar, CA 2002 Proteolytic activity of commercial rennets and pure enzymes on whey proteins. Milchwissenschaft 57 546550
Carminati, D & Giraffa, G 1992 Evidence and characterization of temperate bacteriophage in Streptococcus salivarius subsp. thermophilus St18. Journal of Dairy Research 59 7179
Carminati, D, Mazzucotelli, G, Giraffa, G & Neviani, E 1997 Incidence of inducible bacteriophage in Lactobacillus helveticus strains isolated from natural whey starter cultures. Journal of Dairy Science 80 15051511
Coffey, A & Ross, P 2002 Bacteriophage-resistance systems in dairy starters strains: molecular analysis to application. Antoine van Leeuwenhoek 82 303321
Davidson, B, Powell, IB & Hillier, AJ 1990 Temperate bacteriophages and lysogeny in lactic acid bacteria. FEMS Microbioogyl Reviews 87 7990
de los Reyes-Gavilán, C, Linsowtin, G, Séchaud, L, Veaux, M & Accolas, J-P 1990 Evidence for a plasmid – linked to restriction – modification system in Lactobacillus delbrueckii. Applied and Environmental Microbiology 56 34123419
Deveau, H, Barrangou, R, Garneau, JE, Labonté, J, Fremaux, C, Boyaval, P, Romero, DA, Horvath, P & Moineau, S 2008 Phage Response to CRISPR-Encoded Resistance in Streptococcus thermophilus. Journal of Bacteriology 190 13901400
Giraffa, G, De Vecchi, P & Reinheimer, JA 1997 Population dynamics of thermophilic lactobacilli in mixed starter whey cultures. Food Research International 302 137140
Giraffa, G & Rosetti, L 2004 Monitoring of the bacterial composition of dairy starter cultures by RAPD-PCR. FEMS Microbiology Letters 237 133138
Josephsen, J & Neve, H 1998 Bacteriophages and lactic acid bacteria. In Lactic Acid Bacteria Microbiology and Functional Aspects, pp. 385436 (Eds Salminen, S & Wright, A von). New York: Marcel Decker Inc
Klaenhammer, TR & Fitzgerald, GF 1994 Bacteriophages and bacteriophage resistance. In Genetics and Biotechnology of Lactic Acid Bacteria, pp. 106158 (Eds Gasson, MJ & de Vos, WN). London: Chapman & Hall
Labrie, S & Moineau, S 2007 Abortive influence mechanisms and prophage sequences significantly influence genetic makeaup of emerging lytic lactococal phages. Journal of Bacteriology 189 14821487
Moineau, S, Tremblay, D & Labrie, S 2002 Phages of lactic acid bacteria: from genomics to industrial applications. American Society for Microbiology News 68 388393
Murray, N 2000 Type I restriction systems: sophisticated molecular machines a legacy of Bertani and Weigle. Microbiology and Molecular Biology Reviews 64 2412434
Neviani, E & Carini, S 1994 Microbiology of Parmesan cheese. Microbiologie Aliments Nutrition 12 18
Quiberoni, A, Guglielmotti, D, Binetti, A & Reinheimer, J 2004 Characterization of three Lactobacillus delbrueckii subsp bulgaricus phages and the physicochemical analysis of phage adsorption. Journal of Applied Microbiology 96 340351
Quiberoni, A, Reinheimer, J & Tailliez, P 1998 Characterization of Lactobacillus helveticus phage resistant mutants by RAPD fingerngerprints and phenotypic parameters. Food Research International 31 537542
Reinheimer, JA, Suárez, VB, Bailo, NB & Zalazar, CA 1995 Microbiological and technological characteristics of natural whey cultures for Argentinian hard-cheese production. Journal of Food Protection 58 7796799
Reinheimer, J, Quiberoni, A, Tailliez, P, Binetti, A & Suárez, V 1996 The lactic acid microflora of natural whey starters used in Argentina. International Dairy Journal 6 869879
Sambrook, J & Russell, DW 2001 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Schouler, C, Clier, F, Lerayer, AL, Ehrlich, DS & Chopin, M-L 1998 A type IC restriction-modification system in Lactococcus lactis. Journal of Bacteriology 180 2407411
Séchaud, L, Callegari, M-L, Rousseau, M, Muller, M-C & Accolas, J-P 1989 Relationship between temperate bacteriophage 0241 and virulent phage 832-B1 of Lactobacillus helveticus. Netherlands Milk and Dairy Journal 43 261277
Séchaud, L, Cluzel, P-J, Rousseau, M, Baumgartner, A & Accolas, J-P 1988 Bacteriophages of lactobacilli. Biochimie 70 401410
Séchaud, L, Rousseau, M, Fayard, B, Callegari, ML, Quénée, P & Accolas, J-P 1992 Comparative study of 35 bacteriophages of Lactobacillus helveticus: morphology and host range. Applied and Environmental Microbiology 58 10111018
Suárez, V, Zago, M, Quiberoni, A, Carminati, D, Giraffa, G & Reinheimer, J 2008 Lysogeny in Lactobacillus delbrueckii strains and characterization of two new temperate prolate-headed bacteriophages. Journal of Applied Microbiology 105 14021411
Svensson, V & Christiansson, A 1991 Methods for phage monitoring. FIL-IDF Bulletin 263 2939
Tock, M & Dryden, D 2005 The biology of restriction and anti-restriction. Current Opinion in Microbiology 8 466472
Van de Guchte, M, Penaud, S, Grimaldi, C, Barbe, V, Bryson, K, Nicolas, P, Robert, C, Oztas, S, Mangenot, S, Couloux, A, Loux, V, Dervyn, R, Bossy, R, Bolotin, A, Batto, JM, Walunas, T, Gibrat, JF, Bessières, P, Weissenbach, J, Ehrlich, SD & Maguin, E 2006 The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proceedings of the National Academy of Sciences of the United States of America 103 92749279
Yamamoto, KR, Alberts, BM, Benzinger, R, Lawhorne, L & Treiber, G 1970 Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology 40 734744


Evidence for the presence of restriction/modification systems in Lactobacillus delbrueckii

  • Viviana Suárez (a1), Miriam Zago (a2), Giorgio Giraffa (a2), Jorge Reinheimer (a1) and Andrea Quiberoni (a1)...


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