Advertisement

Molecular Genetics and Genomics

, Volume 285, Issue 4, pp 297–311 | Cite as

Comparative genomics of Lactobacillus sakei with emphasis on strains from meat

  • O. Ludvig Nyquist
  • Anette McLeod
  • Dag A. BredeEmail author
  • Lars Snipen
  • Ågot Aakra
  • Ingolf F. NesEmail author
Original Paper

Abstract

Lactobacillus sakei is a lactic acid bacterium important in food microbiology mainly due to its ability to ferment and preserve meat. The genome sequence of L. sakei strain 23K has revealed specialized metabolic capacities that reflect the bacterium’s adaption to meat products, and that differentiate it from other LAB. An extensive genomic diversity analysis was conducted to elucidate the core features of the species, and to provide a better comprehension of niche adaptation of the organism. Here, we describe the genomic comparison of 18 strains of L. sakei originating mainly from processed meat against the 23K strain by comparative genome hybridization. Pulsed field gel electrophoresis was used to estimate the genome sizes of the strains, which varied from 1.880 to 2.175 Mb, and the 23K genome was among the smallest. Consequently, a large part of the genome of this strain belongs to a common gene pool invariant in this species. The majority of genes important in adaption to meat products, the ability to flexibly use meat components, and robustness during meat processing and storage were conserved, such as genes involved in nucleoside scavenging, catabolism of arginine, and the ability to cope with changing redox and oxygen levels, which is indicative of the role these genes play in niche specialization within the L. sakei species. Moreover, an additional set of sequenced L. sakei genes beyond the 23K genome was present on the microarray used, and it was demonstrated that all the strains carry remnants of or complete bacteriocin operons. The genomic divergence corresponded mainly to five regions in the 23K genome, which showed features consistent with horizontal gene transfer. Carbohydrate-fermentation profiles of the strains were evaluated in light of the CGH data, and for most substrates, the genotypes were consistent with the phenotypes. We have demonstrated a highly conserved organization of the L. sakei genomes investigated, and the 23K strain is a suitable model organism to study core features of the L. sakei species.

Keywords

Lactobacillus sakei Comparative genomics 

Abbreviations

LAB

Lactic acid bacteria

CGH

Comparative genome hybridization

HGT

Horizontal gene transfer

Notes

Acknowledgments

The authors would like to thank Professor Monique Zagorec, INRA, France, for the invitation to collaborate on production of the L. sakei microarray. We also thank Bjørn E. Kristiansen, the Norwegian Microarray Consortium (NMC), Oslo, for printing of the microarrays. We thank Dr. Dave Ussery, CBS, Denmark, for assistance given for the generation of Fig. 1.

Supplementary material

438_2011_608_MOESM1_ESM.pdf (159 kb)
Supplementary material 1 (PDF 158 kb)
438_2011_608_MOESM2_ESM.doc (44 kb)
Supplementary material 2 (DOC 44.5 kb)
438_2011_608_MOESM3_ESM.doc (102 kb)
Supplementary material 3 (DOC 102 kb)
438_2011_608_MOESM4_ESM.pdf (146 kb)
Supplementary material 4 (PDF 145 kb)

References

  1. Aakra A, Nyquist OL, Snipen L, Reiersen TS, Nes IF (2007) Survey of genomic diversity among Enterococcus faecalis strains by microarray-based comparative genomic hybridization. Appl Environ Microbiol 73:2207–2217PubMedCrossRefGoogle Scholar
  2. Aasen IM, Moretro T, Katla T, Axelsson L, Storro I (2000) Influence of complex nutrients, temperature and pH on bacteriocin production by Lactobacillus sakei CCUG 42687. Appl Microbiol Biotechnol 53:159–166PubMedCrossRefGoogle Scholar
  3. Alpert CA, Crutz-Le Coq AM, Malleret C, Zagorec M (2003) Characterization of a theta-type plasmid from Lactobacillus sakei: a potential basis for low-copy-number vectors in lactobacilli. Appl Environ Microbiol 69:5574–5584PubMedCrossRefGoogle Scholar
  4. Axelsson L, Ahrné S (2000) Lactic acid bacteria. In: Priest FG, Goodfellow M (eds) Applied microbial systematics. Kluwer, Dordrechet, pp 365–386Google Scholar
  5. Axelsson L, Holck A, Birkeland SE, Aukrust T, Blom H (1993) Cloning and nucleotide sequence of a gene from Lactobacillus sake Lb706 necessary for sakacin A production and immunity. Appl Environ Microbiol 59:2868–2875PubMedGoogle Scholar
  6. Axelsson L, Katla T, Bjornslett M, Eijsink VG, Holck A (1998) A system for heterologous expression of bacteriocins in Lactobacillus sake. FEMS Microbiol Lett 168:137–143PubMedCrossRefGoogle Scholar
  7. Berthier F, Ehrlich SD (1999) Genetic diversity within Lactobacillus sakei and Lactobacillus curvatus and design of PCR primers for its detection using randomly amplified polymorphic DNA. Int J Syst Bacteriol 49:997–1007PubMedCrossRefGoogle Scholar
  8. Bredholt S, Nesbakken T, Holck A (1999) Protective cultures inhibit growth of Listeria monocytogenes and Escherichia coli O157:H7 in cooked, sliced, vacuum- and gas-packaged meat. Int J Food Microbiol 53:43–52PubMedCrossRefGoogle Scholar
  9. Bredholt S, Nesbakken T, Holck A (2001) Industrial application of an antilisterial strain of Lactobacillus sakei as a protective culture and its effect on the sensory acceptability of cooked, sliced, vacuum-packaged meats. Int J Food Microbiol 66:191–196PubMedCrossRefGoogle Scholar
  10. Brussow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602PubMedCrossRefGoogle Scholar
  11. Bruyneel B, Vanderwoestyne M, Verstraete W (1989) Lactic acid bacteria—microorganisms able to grow in the absence of iron and copper. Biotechnol Lett 11:401–406CrossRefGoogle Scholar
  12. Cai H, Thompson R, Budinich MF, Broadbent JR, Steele JL (2009) Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Genome Biol Evol 2009:239–257Google Scholar
  13. Canchaya C, Claesson MJ, Fitzgerald GF, van Sinderen D, O’Toole PW (2006) Diversity of the genus Lactobacillus revealed by comparative genomics of five species. Microbiology 152:3185–3196PubMedCrossRefGoogle Scholar
  14. Chaillou S, Champomier-Verges MC, Cornet M, Crutz-Le Coq AM, Dudez AM, Martin V, Beaufils S, Darbon-Rongere E, Bossy R, Loux V, Zagorec M (2005) The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat Biotechnol 23:1527–1533PubMedCrossRefGoogle Scholar
  15. Chaillou S, Daty M, Baraige F, Dudez AM, Anglade P, Jones R, Alpert CA, Champomier-Verges MC, Zagorec M (2009) Intraspecies genomic diversity and natural population structure of the meat-borne lactic acid bacterium Lactobacillus sakei. Appl Environ Microbiol 75:970–980PubMedCrossRefGoogle Scholar
  16. Champomier Verges MC, Zuniga M, Morel-Deville F, Perez-Martinez G, Zagorec M, Ehrlich SD (1999) Relationships between arginine degradation, pH and survival in Lactobacillus sakei. FEMS Microbiol Lett 180:297–304PubMedCrossRefGoogle Scholar
  17. Champomier-Verges MC, Chaillou S, Cornet M, Zagorec M (2001) Lactobacillus sakei: recent developments and future prospects. Res Microbiol 152:839–848PubMedCrossRefGoogle Scholar
  18. Champomier-Verges MC, Chaillou S, Cornet M, Zagorec M (2002) Erratum to “Lactobacillus sakei: recent developments and future prospects” [Research in Microbiology 152 (2001) 839]. Res Microbiol 153:115–123PubMedCrossRefGoogle Scholar
  19. Cheetham BF, Katz ME (1995) A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol Microbiol 18:201–208PubMedCrossRefGoogle Scholar
  20. Chen YT, Liao TL, Wu KM, Lauderdale TL, Yan JJ, Huang IW, Lu MC, Lai YC, Liu YM, Shu HY, Wang JT, Su IJ, Tsai SF (2009) Genomic diversity of citrate fermentation in Klebsiella pneumoniae. BMC Microbiol 9:168PubMedCrossRefGoogle Scholar
  21. Chiaramonte F, Blugeon S, Chaillou S, Langella P, Zagorec M (2009) Behavior of the meat-borne bacterium Lactobacillus sakei during its transit through the gastrointestinal tracts of axenic and conventional mice. Appl Environ Microbiol 75:4498–4505PubMedCrossRefGoogle Scholar
  22. Chiaramonte F, Anglade P, Baraige F, Gratadoux JJ, Langella P, Champomier-Verges MC, Zagorec M (2010) Analysis of Lactobacillus sakei mutants selected after adaptation to the gastrointestinal tract of axenic mice. Appl Environ Microbiol 76:2932–2939PubMedCrossRefGoogle Scholar
  23. Claesson MJ, van Sinderen D, O’Toole PW (2007) The genus Lactobacillus—a genomic basis for understanding its diversity. FEMS Microbiol Lett 269:22–28PubMedCrossRefGoogle Scholar
  24. Condon S (1987) Responses of lactic acid bacteria to oxygen. FEMS Microbiol Rev 46:269–280CrossRefGoogle Scholar
  25. Cortez D, Forterre P, Gribaldo S (2009) A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol 10:R65PubMedCrossRefGoogle Scholar
  26. Dal Bello F, Walter J, Hammes WP, Hertel C (2003) Increased complexity of the species composition of lactic acid bacteria in human feces revealed by alternative incubation condition. Microb Ecol 45:455–463PubMedCrossRefGoogle Scholar
  27. Danielsen M (2002) Characterization of the tetracycline resistance plasmid pMD5057 from Lactobacillus plantarum 5057 reveals a composite structure. Plasmid 48:98–103PubMedCrossRefGoogle Scholar
  28. Daubin V, Lerat E, Perriere G (2003) The source of laterally transferred genes in bacterial genomes. Genome Biol 4:R57PubMedCrossRefGoogle Scholar
  29. De Man JC, Rogosa M, Shape ME (1960) A medium for the cultivation of lactobacilli. J Appl Microbiol 23:130–135CrossRefGoogle Scholar
  30. Dong QJ, Wang Q, Xin YN, Li N, Xuan SY (2009) Comparative genomics of Helicobacter pylori. World J Gastroenterol 15:3984–3991PubMedCrossRefGoogle Scholar
  31. Dudez AM, Chaillou S, Hissler L, Stentz R, Champomier-Verges MC, Alpert CA, Zagorec M (2002) Physical and genetic map of the Lactobacillus sakei 23K chromosome. Microbiology 148:421–431PubMedGoogle Scholar
  32. Duhutrel P, Bordat C, Wu TD, Zagorec M, Guerquin-Kern JL, Champomier-Verges MC (2010) Iron sources used by the nonpathogenic lactic acid bacterium Lactobacillus sakei as revealed by electron energy loss spectroscopy and secondary-ion mass spectrometry. Appl Environ Microbiol 76:560–565PubMedCrossRefGoogle Scholar
  33. Duwat P, Sourice S, Cesselin B, Lamberet G, Vido K, Gaudu P, Le Loir Y, Violet F, Loubiere P, Gruss A (2001) Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 183:4509–4516PubMedCrossRefGoogle Scholar
  34. Eijsink VG, Brurberg MB, Middelhoven PH, Nes IF (1996) Induction of bacteriocin production in Lactobacillus sake by a secreted peptide. J Bacteriol 178:2232–2237PubMedGoogle Scholar
  35. Garriga M, Hugas M, Aymerich T, Monfort JM (1993) Bacteriocinogenic activity of lactobacilli from fermented sausages. J Appl Bacteriol 75:142–148PubMedGoogle Scholar
  36. Gevers D, Danielsen M, Huys G, Swings J (2003) Molecular characterization of tet(M) genes in Lactobacillus isolates from different types of fermented dry sausage. Appl Environ Microbiol 69:1270–1275PubMedCrossRefGoogle Scholar
  37. Hagen BF, Naes H, Holck AL (2000) Meat starters have individual requirements for Mn2+. Meat Sci 55:161–168CrossRefGoogle Scholar
  38. Hallin PF, Binnewies TT, Ussery DW (2008) The genome BLASTatlas—a GeneWiz extension for visualization of whole-genome homology. Mol Biosyst 4:363–371PubMedCrossRefGoogle Scholar
  39. Hammes WP, Hertel C (1998) New developments in meat starter cultures. Meat Sci 49:125–138CrossRefGoogle Scholar
  40. Hammes WP, Vogel RF (1995) The genus Lactobacillus. In: Wood BJB, Hilzapfel WH (eds) The genera of lactic acid bacteria, vol 2. Blackie Academic, Professional, Glasgow, pp 19–54Google Scholar
  41. Hertel C, Schmidt G, Fischer M, Oellers K, Hammes WP (1998) Oxygen-dependent regulation of the expression of the catalase gene katA of Lactobacillus sakei LTH677. Appl Environ Microbiol 64:1359–1365PubMedGoogle Scholar
  42. Holck AL, Axelsson L, Huhne K, Krockel L (1994) Purification and cloning of sakacin 674, a bacteriocin from Lactobacillus sake Lb674. FEMS Microbiol Lett 115:143–149PubMedCrossRefGoogle Scholar
  43. Hugas M, Garriga M, Aymerich T, Monfort JM (1995) Inhibition of Listeria in dry fermented sausages by the bacteriocinogenic Lactobacillus sake CTC 494. J Appl Bacteriol 79:322–330Google Scholar
  44. Jacquot R (1961) Organic constituents of fish and other aquatic animal foods. In: Borgstrom G (ed) Fish as food, vol 1. Academic, San Diego, pp 145–209Google Scholar
  45. Katagiri H, Kitahara K, Fukami K (1934) The characteristics of the lactic acid bacteria isolated from moto, yeast mashes for sake manufacture. Part IV. Classification of the lactic acid bacteria. Bull Agric Chem Soc Jpn 10:156–157Google Scholar
  46. Klaenhammer T, Altermann E, Arigoni F, Bolotin A, Breidt F, Broadbent J, Cano R, Chaillou S, Deutscher J, Gasson M, van de Guchte M, Guzzo J, Hartke A, Hawkins T, Hols P, Hutkins R, Kleerebezem M, Kok J, Kuipers O, Lubbers M, Maguin E, McKay L, Mills D, Nauta A, Overbeek R, Pel H, Pridmore D, Saier M, van Sinderen D, Sorokin A, Steele J, O’Sullivan D, de Vos W, Weimer B, Zagorec M, Siezen R (2002) Discovering lactic acid bacteria by genomics. Antonie Van Leeuwenhoek 82:29–58PubMedCrossRefGoogle Scholar
  47. Klein G, Dicks LMT, Pack A, Hack B, Zimmerman K, Dellaglio F, Reuter G (1996) Emended description of Lactobacillus sake (Katahiri, Katahara and Fukami) and Lactobacillus curvatus (Abo-Elnega Kandler): Numerical classification revealed by protein fingerprinting and identification based on biochemical patterns and DNA–DNA hybridizations. Int J Syst Bacteriol 46:367–376CrossRefGoogle Scholar
  48. Knauf HJ, Vogel RF, Hammes WP (1992) Cloning, sequence, and phenotypic expression of katA, which encodes the catalase of Lactobacillus sake LTH677. Appl Environ Microbiol 58:832–839PubMedGoogle Scholar
  49. Koort J, Vandamme P, Schillinger U, Holzapfel W, Bjorkroth J (2004) Lactobacillus curvatus subsp. melibiosus is a later synonym of Lactobacillus sakei subsp. carnosus. Int J Syst Evol Microbiol 54:1621–1626PubMedCrossRefGoogle Scholar
  50. Kralj S, van Geel-Schutten GH, Dondorff MM, Kirsanovs S, van der Maarel MJ, Dijkhuizen L (2004) Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150:3681–3690PubMedCrossRefGoogle Scholar
  51. Lawrence JG, Ochman H (1997) Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44:383–397PubMedCrossRefGoogle Scholar
  52. Leistner L (2000) Basic aspects of food preservation by hurdle technology. Int J Food Microbiol 55:181–186PubMedCrossRefGoogle Scholar
  53. Leroi F, Joffraud JJ, Chevalier F, Cardinal M (1998) Study of the microbial ecology of cold-smoked salmon during storage at 8°C. Int J Food Microbiol 39:111–121PubMedCrossRefGoogle Scholar
  54. Leroy F, de Vuyst L (1999) The presence of salt and a curing agent reduces bacteriocin production by Lactobacillus sakei CTC 494, a potential starter culture for sausage fermentation. Appl Environ Microbiol 65:5350–5356PubMedGoogle Scholar
  55. Leroy F, De Vuyst L (2000) Sakacins. In: Naidu AS (ed) Natural food antimicrobial systems. CRC Press, Boca Raton, pp 589–610Google Scholar
  56. Lyhs U, Bjorkroth J, Korkeala H (1999) Characterisation of lactic acid bacteria from spoiled, vacuum-packaged, cold-smoked rainbow trout using ribotyping. Int J Food Microbiol 52:77–84PubMedCrossRefGoogle Scholar
  57. Magni C, de Mendoza D, Konings WN, Lolkema JS (1999) Mechanism of citrate metabolism in Lactococcus lactis: resistance against lactate toxicity at low pH. J Bacteriol 181:1451–1457PubMedGoogle Scholar
  58. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Diaz-Muniz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103:15611–15616PubMedCrossRefGoogle Scholar
  59. Mathiesen G, Huehne K, Kroeckel L, Axelsson L, Eijsink VG (2005) Characterization of a new bacteriocin operon in sakacin P-producing Lactobacillus sakei, showing strong translational coupling between the bacteriocin and immunity genes. Appl Environ Microbiol 71:3565–3574PubMedCrossRefGoogle Scholar
  60. McLeod A, Nyquist OL, Snipen L, Naterstad K, Axelsson L (2008) Diversity of Lactobacillus sakei strains investigated by phenotypic and genotypic methods. Syst Appl Microbiol 31:393–403PubMedCrossRefGoogle Scholar
  61. McLeod A, Zagorec M, Champomier Verges MC, Naterstad K, Axelsson L (2010) Primary metabolism in Lactobacillus sakei by proteomic analysis. BMC Microbiol 10:120PubMedCrossRefGoogle Scholar
  62. Molenaar D, Bringel F, Schuren FH, de Vos WM, Siezen RJ, Kleerebezem M (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. J Bacteriol 187:6119–6127PubMedCrossRefGoogle Scholar
  63. Moretro T, Naterstad K, Wang E, Aasen IM, Chaillou S, Zagorec M, Axelsson L (2005) Sakacin P non-producing Lactobacillus sakei strains contain homologues of the sakacin P gene cluster. Res Microbiol 156:949–960PubMedCrossRefGoogle Scholar
  64. Mortvedt CI, Nissen-Meyer J, Sletten K, Nes IF (1991) Purification and amino acid sequence of lactocin S, a bacteriocin produced by Lactobacillus sake L45. Appl Environ Microbiol 57:1829–1834PubMedGoogle Scholar
  65. Murray AE, Lies D, Li G, Nealson K, Zhou J, Tiedje JM (2001) DNA/DNA hybridization to microarrays reveals gene-specific differences between closely related microbial genomes. Proc Natl Acad Sci USA 98:9853–9858PubMedCrossRefGoogle Scholar
  66. Nigatu A (2000) Evaluation of numerical analyses of RAPD and API 50 CH patterns to differentiate Lactobacillus plantarum, L. fermentum, L. rhamnosus, L. sake, L. parabuchneri, L. gallinarum, L. casei, Weissella minor and related taxa isolated from kocho and tef. J Appl Microbiol 89:969–978PubMedCrossRefGoogle Scholar
  67. O’Sullivan O, O’Callaghan J, Sangrador-Vegas A, McAuliffe O, Slattery L, Kaleta P, Callanan M, Fitzgerald GF, Ross RP, Beresford T (2009) Comparative genomics of lactic acid bacteria reveals a niche-specific gene set. BMC Microbiol 9:50PubMedCrossRefGoogle Scholar
  68. Obst M, Meding ER, Vogel RF, Hammes WP (1995) Two genes encoding the beta-galactosidase of Lactobacillus sake. Microbiology 141:3059–3066PubMedCrossRefGoogle Scholar
  69. Ouwehand AC, Salminen S, Isolauri E (2002) Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82:279–289PubMedCrossRefGoogle Scholar
  70. Pfeiler EA, Klaenhammer TR (2007) The genomics of lactic acid bacteria. Trends Microbiol 15:546–553PubMedCrossRefGoogle Scholar
  71. Riley MA, Wertz JE (2002) Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie 84:357–364PubMedCrossRefGoogle Scholar
  72. Rodriguez JM, Cintas LM, Casaus P, Suarez A, Hernandez PE (1995) PCR detection of the lactocin S structural gene in bacteriocin-producing lactobacilli from meat. Appl Environ Microbiol 61:2802–2805PubMedGoogle Scholar
  73. Rodriguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pasic L, Thingstad TF, Rohwer F, Mira A (2009) Explaining microbial population genomics through phage predation. Nat Rev Microbiol 7:828–836PubMedCrossRefGoogle Scholar
  74. Schillinger U, Lucke FK (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55:1901–1906PubMedGoogle Scholar
  75. Schillinger U, Lücke F-K (1987) Identification of lactobacilli from meat and meat products. Food Microbiol 4:199–208CrossRefGoogle Scholar
  76. Siezen R, Boekhorst J, Muscariello L, Molenaar D, Renckens B, Kleerebezem M (2006) Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific gram-positive bacteria. BMC Genomics 7:126PubMedCrossRefGoogle Scholar
  77. Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HT, Rademaker JL, Starrenburg MJ, Kleerebezem M, Molenaar D, van Hylckama Vlieg JE (2010) Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12:758–773PubMedCrossRefGoogle Scholar
  78. Simon L, Fremaux C, Cenatiempo Y, Berjeaud JM (2002) Sakacin g, a new type of antilisterial bacteriocin. Appl Environ Microbiol 68:6416–6420PubMedCrossRefGoogle Scholar
  79. Skaugen M, Abildgaard CI, Nes IF (1997) Organization and expression of a gene cluster involved in the biosynthesis of the lantibiotic lactocin S. Mol Gen Genet 253:674–686PubMedCrossRefGoogle Scholar
  80. Skaugen M, Andersen EL, Christie VH, Nes IF (2002) Identification, characterization, and expression of a second, bicistronic, operon involved in the production of lactocin S in Lactobacillus sakei L45. Appl Environ Microbiol 68:720–727PubMedCrossRefGoogle Scholar
  81. Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31:265–273PubMedCrossRefGoogle Scholar
  82. Snipen L, Nyquist OL, Solheim M, Aakra A, Nes IF (2009) Improved analysis of bacterial CGH data beyond the log-ratio paradigm. BMC Bioinformatics 10:91PubMedCrossRefGoogle Scholar
  83. Solheim M, Aakra A, Snipen LG, Brede DA, Nes IF (2009) Comparative genomics of Enterococcus faecalis from healthy Norwegian infants. BMC Genomics 10:194PubMedCrossRefGoogle Scholar
  84. Stentz R, Zagorec M (1999) Ribose utilization in Lactobacillus sakei: analysis of the regulation of the rbs operon and putative involvement of a new transporter. J Mol Microbiol Biotechnol 1:165–173PubMedGoogle Scholar
  85. Stentz R, Cornet M, Chaillou S, Zagorec M (2001) Adaption of Lactobacillus sakei to meat: a new regulatory mechanism of ribose utilization? INRA, EDP Sciences 81:131–138Google Scholar
  86. Tichaczek PS, Vogel RF, Hammes WP (1994) Cloning and sequencing of sakP encoding sakacin P, the bacteriocin produced by Lactobacillus sake LTH 673. Microbiology 140:361–367PubMedCrossRefGoogle Scholar
  87. Torriani S, Van Reenen GA, Klein G, Reuter G, Dellaglio F, Dicks LM (1996) Lactobacillus curvatus subsp. curvatus subsp. nov. and Lactobacillus curvatus subsp. melibiosus subsp. nov. and Lactobacillus sake subsp. sake subsp. nov. and Lactobacillus sake subsp. carnosus subsp. nov., new subspecies of Lactobacillus curvatus Abo-Elnaga and Kandler 1965 and Lactobacillus sake Katagiri, Kitahara, and Fukami 1934 (Klein et al. 1996, emended descriptions), respectively. Int J Syst Bacteriol 46:1158–1163PubMedCrossRefGoogle Scholar
  88. Vaughan A, Eijsink VG, Van Sinderen D (2003) Functional characterization of a composite bacteriocin locus from malt isolate Lactobacillus sakei 5. Appl Environ Microbiol 69:7194–7203PubMedCrossRefGoogle Scholar
  89. Vermeiren L, Devlieghere F, Debevere J (2004) Evaluation of meat born lactic acid bacteria as protective cultures for biopreservation of cooked meat products. Int J Food Microbiol 96:149–164PubMedCrossRefGoogle Scholar
  90. Vogel RF, Lohmann M, Nguyen M, Weller AN, Hammes WP (1993) Molecular characterization of Lactobacillus curvatus and L. sake isolated from sauerkraut and their application in sausage fermentations. J Appl Bacteriol 74:295–300PubMedGoogle Scholar
  91. Weinberg ED (1997) The Lactobacillus anomaly: total iron abstinence. Perspect Biol Med 40:578–583PubMedGoogle Scholar
  92. Zuniga M, Champomier-Verges M, Zagorec M, Perez-Martinez G (1998) Structural and functional analysis of the gene cluster encoding the enzymes of the arginine deiminase pathway of Lactobacillus sake. J Bacteriol 180:4154–4159PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Laboratory of Microbial Gene Technology and Food Microbiology, Department of Chemistry, Biotechnology and Food SciencesNorwegian University of Life SciencesÅsNorway
  2. 2.Biostatistics, Department of Chemistry, Biotechnology and Food SciencesNorwegian University of Life SciencesÅsNorway
  3. 3.Nofima Mat ASNorwegian Institute of Food, Fisheries and Aquaculture ResearchÅsNorway

Personalised recommendations