Comparative genomic and functional analysis of Lactobacillus casei and Lactobacillus rhamnosus strains marketed as probiotics

Applied and Environmental Microbiology

Volumn 79, Issue 6, 2013, Pages 1923-1933

  Douillard, François P ^a   Ribbera, Angela ^a,b   Järvinen, Hanna M ^c   Kant, Ravi ^a   Pietilä, Taija E ^a   Randazzo, Cinzia ^d   Paulin, Lars ^e   Laine, Pia K ^e   Caggia, Cinzia ^d   von Ossowski, Ingemar ^a   Reunanen, Justus ^a   Satokari, Reetta ^a,f   Salminen, Seppo ^f   Palva, Airi ^a   de Vosa, Willem M ^a,b,c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF CATANIA   (Italy)

^e UNIVERSITY OF HELSINKI   (Finland)

^f UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPARATIVE GENOMIC; GENE CLUSTERS; GENOMIC STABILITY; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS STRAIN; LACTOBACILLUS STRAINS; METABOLIC CAPACITIES; PHENOTYPIC ANALYSIS; PROBIOTIC PRODUCTS; PROBIOTICS; REPORTER CELL LINE; TOLL-LIKE RECEPTOR 2; TRANSCRIPTION INITIATION;

BACILLI; BODY FLUIDS; CARBOHYDRATES; CELL CULTURE; COMMERCE; FOOD PRODUCTS; GENES; TRANSCRIPTION;

STRAIN;

PROBIOTIC AGENT;

BACTERIUM; COMPARATIVE STUDY; GENE EXPRESSION; GENOME; PHENOTYPE; PROBIOTICS; SIGNAL;

ARTICLE; BACTERIUM IDENTIFICATION; COMPARATIVE STUDY; GENETIC VARIABILITY; GENETICS; GENOTYPE; IMMUNOLOGY; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; METABOLISM; PHENOTYPE; PHYSIOLOGY;

BACTERIAL TYPING TECHNIQUES; GENETIC VARIATION; GENOTYPE; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; PHENOTYPE; PROBIOTICS;

EID: 84874795543     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03467-12     Document Type: Article

References (58)

1. Kandler O. 1983. Carbohydrate metabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 49:209 -224.
2. de Vos WM. 2011. Systems solutions by lactic acid bacteria: from paradigms to practice. Microb. Cell Fact. 10(Suppl 1):S2. doi:10.1186/1475 -2859-10-S1-S2.
3. FAO/WHO. 2002. Guidelines for the evaluation of probiotics in food. World Health Organization, Geneva, Switzerland.
4. Kant R, Blom J, Palva A, Siezen RJ, de Vos WM. 2011. Comparative genomics of Lactobacillus. Microb. Biotechnol. 4:323-332.
5. Saxelin M, Tynkkynen S, Mattila-Sandholm T, de Vos WM. 2005. Probiotic and other functional microbes: from markets to mechanisms. Curr. Opin. Biotechnol. 16:204 -211.
6. Marco ML, Pavan S, Kleerebezem M. 2006. Towards understanding molecular modes of probiotic action. Curr. Opin. Biotechnol. 17:204- 210.
7. Kalliomaki M, Salminen S, Poussa T, Arvilommi H, Isolauri E. 2003. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361:1869 -1871.
8. Szajewska H, Mrukowicz JZ. 2001. Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J. Pediatr. Gastroenterol. Nutr. 33(Suppl 2):S17-S25. doi:10.1097 /00005176-200110002-00004.
9. Ventura M, O'Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, O'Toole PW. 2009. Genome-scale analyses of healthpromoting bacteria: probiogenomics. Nat. Rev. Microbiol. 7:61-71.
10. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx APA, Lebeer S, De Keersmaecker SCJ, Vanderleyden J, Hamalainen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjarvi T, Auvinen P, de Vos WM. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc. Natl. Acad. Sci. U. S. A. 106:17193- 17198.
11. Lebeer S, Claes IJJ, Verhoeven TLA, Vanderleyden J, De Keersmaecker SCJ. 2011. Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb. Biotechnol. 4:368 -374.
12. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB. 2007. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132:562-575.
13. Claes IJ, Schoofs G, Regulski K, Courtin P, Chapot-Chartier MP, Rolain T, Hols P, von Ossowski I, Reunanen J, de Vos WM, Palva A, Vanderleyden J, De Keersmaecker SC, Lebeer S. 2012. Genetic and biochemical characterization of the cell wall hydrolase activity of the major secreted protein of Lactobacillus rhamnosus GG. PLoS One 7:e31588. doi:10.1371 /journal.pone.0031588.
14. Lebeer S, Claes IJ, Balog CI, Schoofs G, Verhoeven TL, Nys K, von Ossowski I, de Vos WM, Tytgat HL, Agostinis P, Palva A, Van Damme EJ, Deelder AM, De Keersmaecker SC, Wuhrer M, Vanderleyden J. 2012. The major secreted protein MspI/p75 is O-glycosylated in Lactobacillus rhamnosus GG. Microb. Cell Fact. 11:15. doi:10.1186/1475 -2859-11-15.
15. von Ossowski I, Satokari R, Reunanen J, Lebeer S, De Keersmaecker SCJ, Vanderleyden J, de Vos WM, Palva A. 2011. Functional characterization of a mucus-specific LPXTG surface adhesin from probiotic Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 77:4465- 4472.
16. Velez MP, Petrova MI, Lebeer S, Verhoeven TLA, Claes I, Lambrichts I, Tynkkynen S, Vanderleyden J, De Keersmaecker SCJ. 2010. Characterization of MabA, a modulator of Lactobacillus rhamnosus GG adhesion and biofilm formation. FEMS Immunol. Med. Microbiol. 59:386 -398.
17. Reunanen J, von Ossowski I, Hendrickx APA, Palva A, de Vos WM. 2012. Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 78:2337-2344.
18. von Ossowski I, Reunanen J, Satokari R, Vesterlund S, Kankainen M, Huhtinen H, Tynkkynen S, Salminen S, de Vos WM, Palva A. 2010. Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl. Environ. Microbiol. 76:2049- 2057.
19. Bauerl C, Perez-Martinez G, Yan F, Polk DB, Monedero V. 2010. Functional analysis of the p40 and p75 proteins from Lactobacillus casei BL23. J. Mol. Microbiol. Biotechnol. 19:231-241.
20. Regulski K, Courtin P, Meyrand M, Claes IJ, Lebeer S, Vanderleyden J, Hols P, Guillot A, Chapot-Chartier MP. 2012. Analysis of the peptidoglycan hydrolase complement of Lactobacillus casei and characterization of the major gamma-D-glutamyl-L-lysyl-endopeptidase. PLoS One 7:e32301. doi:10.1371/journal.pone.0032301.
21. 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. U. S. A. 103:15611-15616.
22. Maze A, Boel G, Zuniga M, Bourand A, Loux V, Yebra MJ, Monedero V, Correia K, Jacques N, Beaufils S, Poncet S, Joyet P, Milohanic E, Casaregola S, Auffray Y, Perez-Martinez G, Gibrat JF, Zagorec M, Francke C, Hartke A, Deutscher J. 2010. Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J. Bacteriol. 192:2647-2648.
23. Zhang WY, Yu DL, Sun ZH, Wu RN, Chen X, Chen W, Meng H, Hu SN, Zhang HP. 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.
24. Chen C, Ai LZ, Zhou FF, Wang L, Zhang H, Chen W, Guo BH. 2011. Complete genome sequence of the probiotic bacterium Lactobacillus casei LC2W. J. Bacteriol. 193:3419 -3420.
25. Hochwind K, Weinmaier T, Schmid M, van Hemert S, Hartmann A, Rattei T, Rothballer M. 2012. Draft genome sequence of Lactobacillus casei W56. J. Bacteriol. 194:6638. doi:10.1128/JB.01386-12.
26. Ai LZ, Chen C, Zhou FF, Wang L, Zhang H, Chen W, Guo BH. 2011. Complete genome sequence of the probiotic strain Lactobacillus casei BD-II. J. Bacteriol. 193:3160 -3161.
27. Broadbent J, Neeno-Eckwall E, Stahl B, Tandee K, Cai H, Morovic W, Horvath P, Heidenreich J, Perna N, Barrangou R, Steele J. 2012. Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. BMC Genomics 13:533. doi:10.1186 /1471-2164-13-533.
28. Cai H, Thompson R, Budinich M, Broadbent JR, Steele JL. 2009. Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Genome Biol. Evol. 1:239- 257.
29. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, Poiret S, Dewulf J, Brassart D, Mercenier A, Pot B. 2007. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 13:236 -243.
30. Munoz-Provencio D, Perez-Martinez G, Monedero V. 2010. Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J. Appl. Microbiol. 108:1050 -1059.
31. Alcántara C, Revilla-Guarinos A, Zúñiga M. 2011. Influence of twocomponent signal transduction systems of Lactobacillus casei BL23 on tolerance to stress conditions. Appl. Environ. Microbiol. 77:1516 -1519.
32. Alcántara C, Zúñiga M. 2012. Proteomic and transcriptomic analysis of the response to bile stress of Lactobacillus casei BL23. Microbiology 158: 1206-1218.
33. Broadbent JR, Larsen RL, Deibel V, Steele JL. 2010. Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J. Bacteriol. 192:2445-2458.
34. Hamon E, Horvatovich P, Bisch M, Bringel F, Marchioni E, Aoude- Werner D, Ennahar S. 2012. Investigation of biomarkers of bile tolerance in Lactobacillus casei using comparative proteomics. J. Proteome Res. 11: 109-118.
35. Hansen PA, Lessel EF. 1971. Lactobacillus casei (Orla-Jensen) comb. nov. Int. J. Syst. Bacteriol. 21:69 -71.
36. Ventura M, Canchaya C, Meylan V, Klaenhammer TR, Zink R. 2003. Analysis, characterization, and loci of the tuf genes in Lactobacillus and Bifidobacterium species and their direct application for species identification. Appl. Environ. Microbiol. 69:6908-6922.
37. Vesterlund S, Paltta J, Karp M, Ouwehand AC. 2005. Measurement of bacterial adhesion-in vitro evaluation of different methods. J. Microbiol. Methods 60:225-233.
38. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078 -2079.
39. Kurtz S, Phillippy A, Delcher A, Smoot M, Shumway M, Antonescu C, Salzberg S. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12. doi:10.1186/gb-2004-5-2-r12.
40. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389 -3402.
41. Lerat E, Daubin V, Moran NA. 2003. From gene trees to organismal phylogeny in prokaryotes: the case of the -proteobacteria. PLoS Biol. 1:E19. doi:10.1371/journal.pbio.0000019.
42. Tu WY, Pohl S, Gizynski K, Harwood CR. 2012. The iron-binding protein Dps2 confers peroxide stress resistance on Bacillus anthracis. J. Bacteriol. 194:925-931.
43. Jacobsen CN, Rosenfeldt Nielsen V, Hayford AE, Moller PL, Michaelsen KF, Paerregaard A, Sandstrom B, Tvede M, Jakobsen M. 1999. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl. Environ. Microbiol. 65:4949-4956.
44. Koskenniemi K, Laakso K, Koponen J, Kankainen M, Greco D, Auvinen P, Savijoki K, Nyman TA, Surakka A, Salusjarvi T, de Vos WM, Tynkkynen S, Kalkkinen N, Varmanen P. 2011. Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG. Mol. Cell. Proteomics 10:M110.002741. doi:10.1074 /mcp.M110.002741.
45. Ouwehand AC, Kirjavainen PV, Grönlund M-M, Isolauri E, Salminen SJ. 1999. Adhesion of probiotic micro-organisms to intestinal mucus. Int. Dairy J. 9:623- 630.
46. Lebeer S, Claes I, Tytgat HL, Verhoeven TL, Marien E, von Ossowski I, Reunanen J, Palva A, Vos WM, Keersmaecker SC, Vanderleyden J. 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.
47. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O'Brien F, Flynn K, Casey PG, Moreno Munoz JA, Kearney B, Houston AM, O'Mahony C, Higgins DG, Shanahan F, Palva A, de Vos WM, Fitzgerald GF, Ventura M, O'Toole PW, van Sinderen D. 2011. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc. Natl. Acad. Sci. U. S. A. 108:11217-11222.
48. Yebra MJ, Veyrat A, Santos MA, Pérez-Martínez G. 2000. Genetics of L-sorbose transport and metabolism in Lactobacillus casei. J. Bacteriol. 182:155-163.
49. Lebeer S, Vanderleyden J, De Keersmaecker SC. 2010. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8:171-184.
50. Bormann Chung CA, Boyd VL, McKernan KJ, Fu Y, Monighetti C, Peckham HE, Barker M. 2010. Whole methylome analysis by ultra-deep sequencing using two-base encoding. PLoS One 5:e9320. doi:10.1371 /journal.pone.0009320.
51. Wang W, Messing J. 2011. High-throughput sequencing of three Lemnoideae (duckweeds) chloroplast genomes from total DNA. PLoS One 6:e24670. doi:10.1371/journal.pone.0024670.
52. Stevens MJA, Molenaar D, de Jong A, De Vos WM, Kleerebezem M. 2010. 54-mediated control of the mannose phosphotransferase system in Lactobacillus plantarum impacts on carbohydrate metabolism. Microbiology 156:695-707.
53. Poirel L, Decousser J-W, Nordmann P. 2003. Insertion sequence ISEcp1B is involved in expression and mobilization of a blaCTX-M -lactamase gene. Antimicrob. Agents Chemother. 47:2938 -2945.
54. Reynolds AE, Mahadevan S, LeGrice SF, Wright A. 1986. Enhancement of bacterial gene expression by insertion elements or by mutation in a CAP-cAMP binding site. J. Mol. Biol. 191:85-95.
55. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, Parkhill J. 2005. ACT: the Artemis comparison tool. Bioinformatics 21: 3422-3423.
56. Krumsiek J, Arnold R, Rattei T. 2007. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026 -1028.
57. Monedero V, Yebra MJ, Poncet S, Deutscher J. 2008. Maltose transport in Lactobacillus casei and its regulation by inducer exclusion. Res. Microbiol. 159:94 -102.
58. Gosalbes MJ, Monedero V, Péresz-Martínez G. 1999. Elements involved in catabolite repression and substrate induction of the lactose operon in Lactobaccillus casei. J. Bacteriol. 181:3928 -3934.