Comparative genome analysis of Lactobacillus casei strains isolated from Actimel and Yakult products reveals marked similarities and points to a common origin

Microbial Biotechnology

Volumn 6, Issue 5, 2013, Pages 576-587

  Douillard, François P ^a   Kant, Ravi ^a   Ritari, Jarmo ^a   Paulin, Lars ^b   Palva, Airi ^a   De Vos, Willem M ^a,c,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; YOGHURT;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATION; CHROMOSOME REARRANGEMENT; CHROMOSOME SUBSTITUTION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA BASE COMPOSITION; DNA SEQUENCE; GENE SEQUENCE; GENETIC RECOMBINATION; GENOME ANALYSIS; GENOME SIZE; INDEL MUTATION; INTESTINE CELL; LACTOBACILLUS CASEI; MISSENSE MUTATION; NONHUMAN; OPERON; PLASMID; SINGLE NUCLEOTIDE POLYMORPHISM; STOP CODON; SYNTENY;

EID: 84882236945     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12062     Document Type: Article

References (67)

1. Ai, L., Chen, C., Zhou, F., Wang, L., Zhang, H., Chen, W., and Guo, B. (2011) Complete genome sequence of the probiotic strain Lactobacillus casei BD-II. J Bacteriol 193: 3160-3161.
2. Alcántara, C., and Zúñiga, M. (2012) Proteomic and transcriptomic analysis of the response to bile stress of Lactobacillus casei BL23. Microbiology 158: 1206-1218.
3. Alikhan, N.-F., Petty, N., Ben Zakour, N., and Beatson, S. (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12: 402.
4. Almeida, C.C., Lorena, S.L., Pavan, C.R., Akasaka, H.M., and Mesquita, M.A. (2012) Beneficial effects of long-term consumption of a probiotic combination of Lactobacillus casei Shirota and Bifidobacterium breve Yakult may persist after suspension of therapy in lactose-intolerant patients. Nutr Clin Pract 27: 247-251.
5. Axelsson, L. (2004) Lactic Acid Bacteria Microbiological and Functional Aspects. New York, USA: Marcel Dekker.
6. Aziz, R., Bartels, D., Best, A., DeJongh, M., Disz, T., Edwards, R., etal. (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
7. Barré, O., Mourlane, F., and Solioz, M. (2007) Copper induction of lactate oxidase of Lactococcus lactis: a novel metal stress response. J Bacteriol 189: 5947-5954.
8. Bauerl, C., Perez-Martinez, G., Yan, F., Polk, D.B., and Monedero, V. (2010) Functional analysis of the p40 and p75 proteins from Lactobacillus casei BL23. J Mol Microbiol Biotechnol 19: 231-241.
9. Broadbent, J.R., Larsen, R.L., Deibel, V., and Steele, J.L. (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192: 2445-2458.
10. Broadbent, J.R., Neeno-Eckwall, E., Stahl, B., Tandee, K., Cai, H., Morovic, W., etal. (2012) Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. BMC Genomics 13: 533.
11. Cai, H., Thompson, R., Budinich, M., Broadbent, J.R., and Steele, J.L. (2009) Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Genome Biol Evol 1: 239-2357.
12. Carver, T., Thomson, N., Bleasby, A., Berriman, M., and Parkhill, J. (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
13. Carver, T., Harris, S.R., Berriman, M., Parkhill, J., and McQuillan, J.A. (2012) Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28: 464-469.
14. Chen, C., Ai, L.Z., Zhou, F.F., Wang, L., Zhang, H., Chen, W., and Guo, B.H. (2011) Complete genome sequence of the probiotic bacterium Lactobacillus casei LC2W. J Bacteriol 193: 3419-3420.
15. Claes, I.J.J., Schoofs, G., Regulski, K., Courtin, P., Chapot-Chartier, M., Rolain, T., etal. (2012) Genetic and biochemical characterization of the cell wall hydrolase activity of the major secreted protein of Lactobacillus rhamnosus GG. PLoS ONE 7: e31588.
16. Collins, M.D., Phillips, B.A., and Zanoni, P. (1989) Deoxyribonucleic acid homology studies of Lactobacillus casei, Lactobacillus paracasei sp. nov., subsp. paracasei and subsp. tolerans, and Lactobacillus rhamnosus sp. nov., comb. nov. Int J Syst Bacteriol 39: 105-108.
17. Cooper, V.S., Vohr, S.H., Wrocklage, S.C., and Hatcher, P.J. (2010) Why genes evolve faster on secondary chromosomes in bacteria. PLoS Comput Biol 6: e1000732.
18. Darling, A.E., Mau, B., and Perna, N.T. (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147.
19. Dellaglio, F., Felis, G.E., and Torriani, S. (2002) The status of the species Lactobacillus casei (Orla-Jensen 1916) Hansen and Lessel 1971 and Lactobacillus paracasei Collins etal. 1989. Request for an opinion. Int J Syst Evol Microbiol 52: 285-287.
20. Dobson, C.M., Chaban, B., Deneer, H., and Ziola, B. (2004) Lactobacillus casei, Lactobacillus rhamnosus, and Lactobacillus zeae isolates identified by sequence signature and immunoblot phenotype. Can J Microbiol 50: 482-488.
21. Douillard, F.P., Ribbera, A., Järvinen, H.M., Kant, R., Pietilä, T.E., Randazzo, C., etal. (2013) Comparative genomic and functional analysis of Lactobacillus casei and Lactobacillus rhamnosus strains marketed as probiotics. Appl Environ Microbiol 79: 1923-1933.
22. Foligne, B., Nutten, S., Grangette, C., Dennin, V., Goudercourt, D., Poiret, S., etal. (2007) Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 13: 236-243.
23. Guillemard, E., Tondu, F., Lacoin, F., and Schrezenmeir, J. (2010) Consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114001 reduces the duration of respiratory infections in the elderly in a randomised controlled trial. Br J Nutr 103: 58-68.
24. Hajela, N., Nair, G.B., Abraham, P., and Ganguly, N.K. (2012) Health impact of probiotics - vision and opportunities. Gut Pathog 4: 1757-4749.
25. Hamon, E., Horvatovich, P., Bisch, M., Bringel, F., Marchioni, E., Aoude-Werner, D., and Ennahar, S. (2012) Investigation of biomarkers of bile tolerance in Lactobacillus casei using comparative proteomics. J Proteome Res 11: 109-118.
26. Hendrickx, A.P.A., Budzik, J.M., Oh, S.-Y., and Schneewind, O. (2011) Architects at the bacterial surface - sortases and the assembly of pili with isopeptide bonds. Nat Rev Microbiol 9: 166-176.
27. Hochwind, K., Weinmaier, T., Schmid, M., van Hemert, S., Hartmann, A., Rattei, T., and Rothballer, M. (2012) Draft genome sequence of Lactobacillus casei W56. J Bacteriol 194: 6638.
28. Horvath, P., and Barrangou, R. (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170.
29. Kalliomaki, M., Salminen, S., Poussa, T., Arvilommi, H., and Isolauri, E. (2003) Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361: 1869-1871.
30. Kandler, O., and Weiss, N. (1986) Bergey's Manual of Systematic Bacteriology. Baltimore, MD, USA: Williams and Wilkins, pp. 1063-1065.
31. Kankainen, M., Paulin, L., Tynkkynen, S., von Ossowski, I., Reunanen, J., Partanen, P., etal. (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci USA 106: 17193-17198.
32. Kingsford, C., Schatz, M., and Pop, M. (2010) Assembly complexity of prokaryotic genomes using short reads. BMC Bioinformatics 11: 21.
33. Klein, G., Pack, A., Bonaparte, C., and Reuter, G. (1998) Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41: 103-125.
34. Kurtz, S., Phillippy, A., Delcher, A., Smoot, M., Shumway, M., Antonescu, C., and Salzberg, S. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.
35. Lebeer, S., Claes, I., Tytgat, H.L., Verhoeven, T.L., Marien, E., von Ossowski, I., etal. (2012) Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl Environ Microbiol 78: 185-193.
36. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., etal. (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
37. Litou, Z.I., Bagos, P.G., Tsirigos, K.D., Liakopoulos, T.D., and Hamodrakas, S.J. (2008) Prediction of cell wall sorting signals in gram-positive bacteria with a hidden markov model: application to complete genomes. J Bioinform Comput Biol 6: 387-401.
38. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., etal. (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103: 15611-15616.
39. Makarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J.J., Charpentier, E., Horvath, P., etal. (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9: 467-477.
40. Marcos, A., Warnberg, J., Nova, E., Gomez, S., Alvarez, A., Alvarez, R., etal. (2004) The effect of milk fermented by yogurt cultures plus Lactobacillus casei DN-114001 on the immune response of subjects under academic examination stress. Eur J Nutr 43: 381-389.
41. Marraffini, L.A., and Sontheimer, E.J. (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11: 181-190.
42. Matsumoto, K., Takada, T., Shimizu, K., Moriyama, K., Kawakami, K., Hirano, K., etal. (2010) Effects of a probiotic fermented milk beverage containing Lactobacillus casei strain Shirota on defecation frequency, intestinal microbiota, and the intestinal environment of healthy individuals with soft stools. J Biosci Bioeng 110: 547-552.
43. Maze, A., Boel, G., Zuniga, M., Bourand, A., Loux, V., Yebra, M.J., etal. (2010) Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J Bacteriol 192: 2647-2648.
44. Mazmanian, S.K., Ton-That, H., and Schneewind, O. (2001) Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol 40: 1049-1057.
45. Munoz-Provencio, D., Perez-Martinez, G., and Monedero, V. (2010) Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J Appl Microbiol 108: 1050-1059.
46. Munoz-Provencio, D., Rodriguez-Diaz, J., Collado, M.C., Langella, P., Bermudez-Humaran, L.G., and Monedero, V. (2012) Functional analysis of the Lactobacillus casei BL23 sortases. Appl Environ Microbiol 78: 8684-8693.
47. Naito, E., Yoshida, Y., Makino, K., Kounoshi, Y., Kunihiro, S., Takahashi, R., etal. (2011) Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. J Appl Microbiol 110: 650-657.
48. Nanno, M., Kato, I., Kobayashi, T., and Shida, K. (2011) Biological effects of probiotics: what impact does Lactobacillus casei Shirota have on us? Int J Immunopathol Pharmacol 24: 45S-50S.
49. Navarre, W.W., and Schneewind, O. (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
50. von Ossowski, I., Satokari, R., Reunanen, J., Lebeer, S., De Keersmaecker, S.C.J., Vanderleyden, J., etal. (2011) Functional characterization of a mucus-specific LPXTG surface adhesin from probiotic Lactobacillus rhamnosus GG. Appl Environ Microbiol 77: 4465-4472.
51. Otto, T.D., Dillon, G.P., Degrave, W.S., and Berriman, M. (2011) RATT: Rapid Annotation Transfer Tool. Nucleic Acids Res 39: 8.
52. Pawlowska, J., Klewicka, E., Czubkowski, P., Motyl, I., Jankowska, I., Libudzisz, Z., etal. (2007) Effect of Lactobacillus casei DN-114001 application on the activity of fecal enzymes in children after liver transplantation. Transplant Proc 39: 3219-3221.
53. Perry, A.M., Ton-That, H., Mazmanian, S.K., and Schneewind, O. (2002) Anchoring of surface proteins to the cell wall of Staphylococcus aureus: III. Lipid II is an in vivo peptidoglycan substrate for sortase-catalyzed surface protein anchoring. J Biol Chem 277: 16241-16248.
54. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
55. Reunanen, J., von Ossowski, I., Hendrickx, A.P., Palva, A., and de Vos, W.M. (2012) Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl Environ Microbiol 78: 2337-2344.
56. Rochat, T., Bermudez-Humaran, L., Gratadoux, J.-J., Fourage, C., Hoebler, C., Corthier, G., and Langella, P. (2007) Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb Cell Fact 6: 22.
57. Rumble, S.M., Lacroute, P., Dalca, A.V., Fiume, M., Sidow, A., and Brudno, M. (2009) SHRiMP: accurate mapping of short color-space reads. PLoS Comput Biol 5: e1000386.
58. Sato, H., Torimura, M., Kitahara, M., Ohkuma, M., Hotta, Y., and Tamura, H. (2012) Characterization of the Lactobacillus casei group based on the profiling of ribosomal proteins coded in S10-spc-alpha operons as observed by MALDI-TOF MS. Syst Appl Microbiol 35: 447-454.
59. Saxelin, M., Tynkkynen, S., Mattila-Sandholm, T., and de Vos, W.M. (2005) Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16: 204-211.
60. Schneewind, O., and Missiakas, D.M. (2012) Protein secretion and surface display in Gram-positive bacteria. Philos Trans R Soc Lond B Biol Sci 367: 1123-1139.
61. Stiles, M.E., and Holzapfel, W.H. (1997) Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol 36: 1-29.
62. Sybesma, W., Molenaar, D., van IJcken, W., Venema, K., and Kort, R. (2013) Genome instability in Lactobacillus rhamnosus GG. Appl Environ Microbiol 79: 2233-2239.
63. Sykora, J., Valeckova, K., Amlerova, J., Siala, K., Dedek, P., Watkins, S., etal. (2005) Effects of a specially designed fermented milk product containing probiotic Lactobacillus casei DN-114 001 and the eradication of H. pylori in children: a prospective randomized double-blind study. J Clin Gastroenterol 39: 692-698.
64. Ventura, M., O'Flaherty, S., Claesson, M.J., Turroni, F., Klaenhammer, T.R., van Sinderen, D., and O'Toole, P.W. (2009) Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7: 61-71.
65. de Vos, W.M. (2011) Systems solutions by lactic acid bacteria: from paradigms to practice. Microb Cell Fact 10: S2.
66. Yan, F., Cao, H., Cover, T.L., Whitehead, R., Washington, M.K., and Polk, D.B. (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132: 562-575.
67. Zhang, W.Y., Yu, D.L., Sun, Z.H., Wu, R.N., Chen, X., Chen, W., etal. (2010) Complete genome sequence of Lactobacillus casei Zhang, a new probiotic strain isolated from traditional homemade koumiss in Inner Mongolia, China. J Bacteriol 192: 5268-5269.