Polymorphisms, chromosomal rearrangements, and mutator phenotype development during experimental evolution of Lactobacillus rhamnosus GG

Applied and Environmental Microbiology

Volumn 82, Issue 13, 2016, Pages 3783-3792

  Douillard, François P ^a   Ribbera, Angela ^a,b   Xiao, Kun ^a   Ritari, Jarmo ^a   Rasinkangas, Pia ^a   Paulin, Lars ^c   Palva, Airi ^a   Hao, Yanling ^b,d   de Vos, Willem M ^a,b,e  

^a UNIVERSITY OF HELSINKI   (Finland)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF HELSINKI   (Finland)

^d CHINA AGRICULTURAL UNIVERSITY   (China)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; FOOD PRODUCTS; GENE ENCODING; LACTIC ACID; SALTS; SHEARING;

CHROMOSOMAL REARRANGEMENT; EXPERIMENTAL EVOLUTION; GENOMIC INTEGRITY; INSERTION SEQUENCES; LACTIC ACID BACTERIA; LACTOBACILLUS RHAMNOSUS; SINGLE NUCLEOTIDE POLYMORPHISMS; STRESS-FREE CONDITIONS;

BACILLI;

BACTERIUM; CHROMOSOME; EVOLUTIONARY BIOLOGY; EXPERIMENTAL STUDY; FOOD INDUSTRY; GENE EXPRESSION; GENETIC ANALYSIS; MUTATION; PHENOTYPE; POLYMORPHISM; PROBIOTICS;

BACTERIA (MICROORGANISMS); LACTOBACILLUS RHAMNOSUS;

PROBIOTIC AGENT; TRANSPOSON;

GENE REARRANGEMENT; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETICS; GENOMIC INSTABILITY; GROWTH, DEVELOPMENT AND AGING; LACTOBACILLUS RHAMNOSUS; MUTATION; PHENOTYPE; TRANSPOSON;

DNA TRANSPOSABLE ELEMENTS; GENE REARRANGEMENT; GENOMIC INSTABILITY; LACTOBACILLUS RHAMNOSUS; MUTATION; PHENOTYPE; POLYMORPHISM, GENETIC; PROBIOTICS; RECOMBINATION, GENETIC;

EID: 84976386639     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00255-16     Document Type: Article

References (48)

1. Silva M, Jacobus NV, Deneke C, Gorbach SL. 1987. Antimicrobial substance from a human Lactobacillus strain. Antimicrob Agents Chemother 31:1231-1233. http://dx.doi.org/10.1128/AAC.31.8.1231.
2. Kalliomäki 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. http://dx.doi.org/10.1016/S0140-6736(03)13490-3.
3. 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. http://dx.doi.org/10.1097/00005176-200110002-00004.
4. Canani RB, Cirillo P, Terrin G, Cesarano L, Spagnuolo MI, De Vincenzo A, Albano F, Passariello A, De Marco G, Manguso F, Guarino A. 2007. Probiotics for treatment of acute diarrhoea in children: randomised clinical trial of five different preparations. BMJ 335:340. http://dx.doi.org/10.1136/bmj.39272.581736.55.
5. Österlund P, Ruotsalainen T, Korpela R, Saxelin M, Ollus A, Valta P, Kouri M, Elomaa I, Joensuu H. 2007. Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: a randomised study. Br J Cancer 97:1028-1034. http://dx.doi.org/10.1038/sj.bjc.6603990.
6. Majamaa H, Isolauri E, Saxelin M, Vesikari T. 1995. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr 20:333-338. http://dx.doi.org/10.1097/00005176-199504000-00012.
7. Arvola T, Laiho K, Torkkeli S, Mykkänen H, Salminen S, Maunula L, Isolauri E. 1999. Prophylactic Lactobacillus GG reduces antibioticassociated diarrhea in children with respiratory infections: a randomized study. Pediatrics 104:e64. http://dx.doi.org/10.1542/peds.104.5.e64.
8. Hojsak I, Snovak N, Abdović S, Szajewska H, Mišak Z, Kolaček S. 2010. LactobacillusGGin the prevention of gastrointestinal and respiratory tract infections in children who attend day care centers: a randomized, doubleblind, placebo-controlled trial. Clin Nutr 29:312-316. http://dx.doi.org/10.1016/j.clnu.2009.09.008.
9. Hatakka K, Savilahti E, Pönkä A, Meurman JH, Poussa T, Näse L, Saxelin M, Korpela R. 2001. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ 322:1327. http://dx.doi.org/10.1136/bmj.322.7298.1327.
10. Nylund L, Satokari R, Nikkilä J, Rajilić-Stojanović M, Kalliomäki M, Isolauri E, Salminen S, de Vos WM. 2013. Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol 13:12. http://dx.doi.org/10.1186/1471-2180-13-12.
11. Elena SF, Lenski RE. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4:457-469. http://dx.doi.org/10.1038/nrg1088.
12. Finkel SE, Kolter R. 1999. Evolution of microbial diversity during prolonged starvation. Proc Natl Acad Sci U S A 96:4023-4027. http://dx.doi.org/10.1073/pnas.96.7.4023.
13. Jerison ER, Desai MM. 2015. Genomic investigations of evolutionary dynamics and epistasis in microbial evolution experiments. Curr Opin Genet Dev 35:33-39. http://dx.doi.org/10.1016/j.gde.2015.08.008.
14. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461:1243-1247. http://dx.doi.org/10.1038/nature08480.
15. Schneider D, Duperchy E, Coursange E, Lenski RE, Blot M. 2000. Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics 156:477-488.
16. Rasinkangas P, Reunanen J, Douillard FP, Ritari J, Uotinen V, Palva A, de Vos WM. 2014. Genomic characterization of non-mucus-adherent derivatives of Lactobacillus rhamnosus GG reveals genes affecting pilus biogenesis. Appl Environ Microbiol 80:7001-7009. http://dx.doi.org/10.1128/AEM.02006-14.
17. Saedler H, Reif HJ, Hu S, Davidson N. 1974. IS2, a genetic element for turn-offand turn-on of gene activity in E. coli. Mol Gen Genet 132:265-289. http://dx.doi.org/10.1007/BF00268569.
18. Douillard FP, Ribbera A, Järvinen HM, Kant R, Pietilä TE, Randazzo C, Paulin L, Laine PK, Caggia C, von Ossowski I, Reunanen J, Satokari R, Salminen S, Palva A, de Vos WM. 2013. Comparative genomic and functional analysis of Lactobacillus casei and Lactobacillus rhamnosus strains marketed as probiotics. Appl Environ Microbiol 79:1923-1933. http://dx.doi.org/10.1128/AEM.03467-12.
19. Schneider D, Lenski RE. 2004. Dynamics of insertion sequence elements during experimental evolution of bacteria. Res Microbiol 155:319-327. http://dx.doi.org/10.1016/j.resmic.2003.12.008.
20. 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, Hämäläinen 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, Salusjärvi 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. http://dx.doi.org/10.1073/pnas.0908876106.
21. Sybesma W, Molenaar D, van IW, Venema K, Kort R. 2013. Genome instability in Lactobacillus rhamnosus GG. Appl Environ Microbiol 79: 2233-2239. http://dx.doi.org/10.1128/AEM.03566-12.
22. Douillard FP, Ribbera A, Kant R, Pietilä TE, Järvinen HM, Messing M, Randazzo CL, Paulin L, Laine P, Ritari J, Caggia C, Lähteinen T, Brouns SJ, Satokari R, von Ossowski I, Reunanen J, Palva A, de Vos WM. 2013. Comparative genomic and functional analysis of 100 Lactobacillus rhamnosus strains and their comparison with strain GG. PLoS Genet 9:e1003683. http://dx.doi.org/10.1371/journal.pgen.1003683.
23. Douillard FP, de Vos WM. 2014. Functional genomics of lactic acid bacteria: from food to health. Microb Cell Fact 13(Suppl 1):S8. http://dx.doi.org/10.1186/1475-2859-13-S1-S8.
24. Bachmann H, Starrenburg MJC, Molenaar D, Kleerebezem M, van Hylckama Vlieg JET. 2012. Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution. Genome Res 22:115-124. http://dx.doi.org/10.1101/gr.121285.111.
25. Lebeer S, Verhoeven TLA, Perea Velez M, Vanderleyden J, De Keersmaecker SCJ. 2007. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73:6768-6775. http://dx.doi.org/10.1128/AEM.01393-07.
26. Lebeer S, Claes I, Tytgat HLP, Verhoeven TLA, Marien E, von Ossowski I, Reunanen J, Palva A, Vos WM, De Keersmaecker SCJ, 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. http://dx.doi.org/10.1128/AEM.06192-11.
27. De Keersmaecker SCJ, Braeken K, Verhoeven TLA, Perea Velez M, Lebeer S, Vanderleyden J, Hols P. 2006. Flow cytometric testing of green fluorescent protein-tagged Lactobacillus rhamnosus GG for response to defensins. Appl Environ Microbiol 72:4923-4930. http://dx.doi.org/10.1128/AEM.02605-05.
28. Douillard FP, Rasinkangas P, von Ossowski I, Reunanen J, Palva A, de Vos WM. 2014. Functional identification of conserved residues involved in Lactobacillus rhamnosus strain GG sortase specificity and pilus biogenesis. J Biol Chem 289:15764-15775. http://dx.doi.org/10.1074/jbc. M113.542332.
29. Ahlroos T, Tynkkynen S. 2009. Quantitative strain-specific detection of Lactobacillus rhamnosus GG in human faecal samples by real-time PCR. J Appl Microbiol 106:506-514. http://dx.doi.org/10.1111/j.1365-2672.2008.04018.x.
30. David M, Dzamba M, Lister D, Ilie L, Brudno M. 2011. SHRiMP2: sensitive yet practical SHort Read Mapping. Bioinformatics 27:1011-1012. http://dx.doi.org/10.1093/bioinformatics/btr046.
31. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352.
32. Delcher AL, Phillippy A, Carlton J, Salzberg SL. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30: 2478-2483. http://dx.doi.org/10.1093/nar/30.11.2478.
33. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, Rance R, Baker S, Maskell DJ, Wain J, Dolecek C, Achtman M, Dougan G. 2008. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 40:987-993. http://dx.doi.org/10.1038/ng.195.
34. Denoeud F, Vergnaud G. 2004. Identification of polymorphic tandem repeats by direct comparison of genome sequence from different bacterial strains: a web-based resource. BMC Bioinformatics 5:4. http://dx.doi.org/10.1186/1471-2105-5-4.
35. Le Fleche P, Hauck Y, Onteniente L, Prieur A, Denoeud F, Ramisse V, Sylvestre P, Benson G, Ramisse F, Vergnaud G. 2001. A tandem repeats database for bacterial genomes: application to the genotyping of Yersinia pestis and Bacillus anthracis. BMC Microbiol 1:2. http://dx.doi.org/10.1186/1471-2180-1-2.
36. Grissa I, Bouchon P, Pourcel C, Vergnaud G. 2008. On-line resources for bacterial micro-evolution studies using MLVA or CRISPR typing. Biochimie 90:660-668. http://dx.doi.org/10.1016/j.biochi.2007.07.014.
37. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205-217. http://dx.doi.org/10.1006/jmbi.2000.4042.
38. Sturn A, Quackenbush J, Trajanoski Z. 2002. Genesis: cluster analysis of microarray data. Bioinformatics 18:207-208. http://dx.doi.org/10.1093/bioinformatics/18.1.207.
39. Yadav P, Harcy V, Argueso JL, Dominska M, Jinks-Robertson S, Kim N. 2014. Topoisomerase I plays a critical role in suppressing genome instability at a highly transcribed G-quadruplex-forming sequence. PLoS Genet 10:e1004839. http://dx.doi.org/10.1371/journal.pgen.1004839.
40. Usongo V, Drolet M. 2014. Roles of type 1A topoisomerases in genome maintenance in Escherichia coli. PLoS Genet 10:e1004543. http://dx.doi.org/10.1371/journal.pgen.1004543.
41. Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998. Rates of spontaneous mutation. Genetics 148:1667-1686.
42. Prasad J, McJarrow P, Gopal P. 2003. Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917-925. http://dx.doi.org/10.1128/AEM.69.2.917-925.2003.
43. Louesdon S, Charlot-Rougé S, Juillard V, Tourdot-Maréchal R, Béal C. 2014. Osmotic stress affects the stability of freeze-dried Lactobacillus buchneri R1102 as a result of intracellular betaine accumulation and membrane characteristics. J Appl Microbiol 117:196-207. http://dx.doi.org/10.1111/jam.12501.
44. Taïbi A, Dabour N, Lamoureux M, Roy D, LaPointe G. 2011. Comparative transcriptome analysis of Lactococcus lactis subsp. cremoris strains under conditions simulating cheddar cheese manufacture. Int J Food Microbiol 146:263-275. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.02.034.
45. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E. 2002. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82:187-216. http://dx.doi.org/10.1023/A:1020631532202.
46. Altermann E, Buck LB, Cano R, Klaenhammer TR. 2004. Identification and phenotypic characterization of the cell-division protein CdpA. Gene 342:189-197. http://dx.doi.org/10.1016/j.gene.2004.08.004.
47. Ardita CS, Mercante JW, Kwon YM, Luo L, Crawford ME, Powell DN, Jones RM, Neish AS. 2014. Epithelial adhesion mediated by pilin SpaC is required for Lactobacillus rhamnosus GG-induced cellular responses. Appl Environ Microbiol 80:5068-5077. http://dx.doi.org/10.1128/AEM.01039-14.
48. 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. http://dx.doi.org/10.1128/AEM.07047-11.