Identification of restriction-modification systems of bifidobacterium animalis subsp. Lactis CNCM I-2494 by SMRT Sequencing and associated methylome analysis

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Motherway, Mary O'Connell ^a   Watson, Debbie ^a   Bottacini, Francesca ^a   Clark, Tyson A ^b   Roberts, Richard J ^c   Korlach, Jonas ^b   Garault, Peggy ^d   Chervaux, Christian ^d   Van Hylckama Vlieg, J E T ^d   Smokvina, Tamara ^d   Van Sinderen, Douwe ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b PACIFIC BIOSCIENCES   (United States)

^c NEW ENGLAND BIOLABS   (United States)

^d DANONE RESEARCH   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID ANALYSIS; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM TRANSFORMATION; BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS; CONTROLLED STUDY; DNA SEQUENCE; GENE LOCUS; GENE SEQUENCE; GENETIC ASSOCIATION; HOMOLOGOUS RECOMBINATION; MOLECULAR CLONING; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; RESTRICTION MAPPING; TRANSPOSON;

EID: 84899678205     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094875     Document Type: Article

References (63)

1. Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, Gómez-Llorente C, Gil A (2012) Probiotic mechanisms of action. Ann Nutr Metab 61: 160-174.
2. Turroni F, Ventura M, Buttó LF, Duranti S, O'Toole PW, O'Connell Motherway M, et al. (2014) Molecular dialogue between the human gut microbiota and the host: A Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71: 183-203.
3. Ventura M, Turroni F, O'Connell Motherway M, MacSharry J, van Sinderen D (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20: 467-476.
4. Agrawal A, Houghton LA, Morris J, Reilly B, Guyonnet D, et al. (2009) Clinical trial: The effects of a fermented milk product containing Bifidobacterium lactis DN- 173 010 on abdominal distension and gastrointestinal transit in irritable bowel syndrome with constipation. Aliment Pharmacol Ther 29: 104-114.
5. Guyonnet D, Schlumberger A, Mhamdi L, Jakob S, Chassany O (2009) Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: A randomised, double-blind, parallel, controlled study. Br J Nutr 102: 1654-1662.
6. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, et al. (2013) Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144: 1394-1401.
7. Veiga P, Gallini CA, Beal C, Michaud M, Delaney ML, DuBois A, et al. (2010) Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc Natl Acad Sci U S A 107: 18132-18137.
8. Agostini S, Goubern M, Tondereau V, Salvador-Cartier C, Bezirard V, et al. (2012) A marketed fermented dairy product containing Bifidobacterium lactis CNCM I-2494 suppresses gut hypersensitivity and colonic barrier disruption induced by acute stress in rats. Neurogastroenterol Motil 376-e172.
9. Ventura M, Turroni F, Lugli GA, van Sinderen D. (2014) Bifidobacteria and humans: our special friends, from ecological to genomics perspectives. J Sci Food Agric 94: 163-168.
10. Chervaux C, Grimaldi C, Bolotin A, Quinquis B, Legrain-Raspaud S, et al. (2011) Genome sequence of the probiotic strain Bifidobacterium animalis subsp. lactis CNCM I-2494. J Bacteriol 193: 5560-5561.
11. Guglielmetti S, Mayo B, Álvarez-Martín P (2013) Mobilome and genetic modification of bifidobacteria. Benef Microbes 4: 143-166.
12. Brancaccio VF, Zhurina DS, Riedel CU (2013) Tough nuts to crack: sitedirected mutagenesis of bifidobacteria remains a challenge. Bioengineered 4: 197-202.
13. Sun Z, Baur A, Zhurina D, Yuan J, Riedel CU. (2012) Accessing the inaccessible: molecular tools for bifidobacteria. Appl Environ Microbiol 78: 5035-5042.
14. Ruiz L, O'Connell-Motherway M, Lanigan N, van Sinderen D (2013) Transposon mutagenesis in Bifidobacterium breve: construction and characterization of a Tn5 transposon mutant library for Bifidobacterium breve UCC2003. PLoS One 8(5):e64699.
15. Law J, Buist G, Haandrikman A, Kok J, Venema G, Leenhouts K (1995) A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177: 7011-7018.
16. O'Connell Motherway M, Fitzgerald GF, Neirynck S, Ryan S, Steidler L, et al. (2008) Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl Environ Microbiol 74(20): 6271-6279.
17. O'Connell Motherway M, O'Driscoll J, Fitzgerald GF, and van Sinderen D (2009) Overcoming the restriction barrier to plasmid transformation and targeted mutagenesis in Bifidobacterium breve UCC2003. Microb Biotechnol 2: 321-332.
18. Yasui K, Kano Y, Tanaka K, Watanabe K, Shimizu-Kadota M, et al. (2009) Improvement of bacterial transformation efficiency using plasmid artificial modification. Nucleic Acids Res 37(1):e3.
19. Kim JY, Wang Y, Park MS, Ji GE. (2010) Improvement of transformation efficiency through in vitro methylation and SacII site mutation of plasmid vector in Bifidobacterium longum MG1. J Microbiol Biotechnol 20: 1022-1026.
20. Pokusaeva K, Neves AR, Zomer A, O'Connell Motherway M, MacSharry J, et al. (2010) Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol 3(3): 311-23.
21. Pokusaeva K, O'Connell-Motherway M, Zomer A, MacSharry J, Fitzgerald GF, et al. (2011) Cellodextrin utilization by Bifidobacterium breve UCC2003. Appl Environ Microbiol 7: 1681-90.
22. O'Connell Motherway M, Kinsella M, Fitzgerald GF, van Sinderen D (2013) Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb Biotechnol 6: 67-79.
23. O'Connell Motherway M, Fitzgerald GF, van Sinderen D (2011) Metabolism of a plant derived galactose-containing polysaccharide by Bifidobacterium breve UCC2003. Microb Biotechnol 4: 403-416.
24. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, et al. (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.
25. O'Connell KJ, O'Connell Motherway M, Hennessey AA, Brodhun F, Ross RP, et al. (2013a) Identification and characterization of an oleate hydratase-encoding gene from Bifidobacterium breve. Bioengineered 4: 313-321.
26. O'Connell KJ, O'Connell Motherway M, O'Callaghan J, Fitzgerald GF, Ross RP, et al. (2013b) Metabolism of four a-glycosidic linkage-containing oligosaccharides by Bifidobacterium breve UCC2003. Appl Environ Microbiol 79: 6280-6292.
27. Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, et al. (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci U S A 109: 2108-2113.
28. Ruiz L, O'Connell-Motherway M, Zomer A, de los Reyes-Gavilán CG, Margolles A, et al. (2012) A bile-inducible membrane protein mediates bifidobacterial bile resistance. Microb Biotechnol 5: 523-535.
29. Alvarez-Martin P, Fernández M, O'Connell-Motherway M, O'Connell KJ, Sauvageot N, et al. (2012) A conserved two-component signal transduction system controls the response to phosphate starvation in Bifidobacterium breve UCC2003. Appl Environ Microbiol 78: 5258-5269.
30. Alvarez-Martin P, O'Connell Motherway M, Turroni F, Foroni E, Ventura M, et al. (2012) A two-component regulatory system controls autoregulated serpin expression in Bifidobacterium breve UCC2003. Appl Environ Microbiol 78: 7032- 7041.
31. Bottacini F, O' Connell Motherway M, Kuczynski J, O'Connell KJ, Serafini F, et al. (2014) Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics In Press.
32. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, et al. (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469: 543-547.
33. Hirayama Y, Sakanaka M, Fukuma H, Murayama H, Kano Y, et al. (2012) Development of a double-crossover markerless gene deletion system in Bifidobacterium longum: functional analysis of the a-galactosidase gene for raffinose assimilation. Appl Environ Microbiol 78: 4984-4994.
34. Sakaguchi K, He J, Tani S, Kano Y, Suzuki T. (2012) A targeted gene knockout method using a newly constructed temperature-sensitive plasmid mediated homologous recombination in Bifidobacterium longum. Appl Microbiol Biotechnol 95: 499-509.
35. Murray IA, Clark TA, Morgan RD, Boitano M, Anton BP, et al. (2012) The methylomes of six bacteria. Nucleic Acids Res 40: 11450-11462.
36. Fang G, Munera D, Friedman DI, Mandlik A, Chao MC, et al. (2012) Genomewide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nat Biotechnol 30: 1232-1239.
37. De Man JC, Rogosa A, Sharpe M E (1960) A medium for the cultivation of lactobacilli. J Appl Bacteriol 23: 130-135.
38. Sambrook J, Fritsch EF, Maniatis T (1989). Molecular cloning a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory.Cold Spring HarborN.Y.
39. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. (2000). Artemis: sequence visualization and annotation. Bioinformatics 10: 944-945.
40. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
41. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
42. Roberts RJ, Vincze T, Posfai J, Macelis D. (2010) REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucl Acids Res 38: D234-D236.
43. O'Riordan K. (1998) Studies on antimicrobial activity and genetic diversity of Bifidobacterium species: molecular characterization of a 5.75 kb plasmid and a chromosomally encoded recA gene homologue from Bifidobacterium breve. Ph.D. National University of IrelandCork, Cork.
44. Wells JM, Wilson PW, Le Page RW (1993) Improved cloning vectors and transformation procedure for Lactococcus lactis. J Appl Bacteriol 74: 629-636. (Pubitemid 23186563)
45. Alvarez-Martín P, O'Connell Motherway M, van Sinderen D, Mayo B. (2007). Functional analysis of the pBC1 replicon from Bifidobacterium catenulatum L48. Appl Microbiol Biotechnol 76: 1395-1402. (Pubitemid 47459785)
46. Rossi M, Brigidi P, Matteuzzi D. (1998) Improved cloning vectors for Bifidobacterium spp. Lett Appl Microbiol 26: 101-104. (Pubitemid 28156824)
47. McGrath S, Fitzgerald GF, van Sinderen D. (2001) Improvement and optimization of two engineered phage resistance mechanisms in Lactococcus lactis. Appl Environ Microbiol 67: 608-616. (Pubitemid 32121348)
48. Wang RF, Kushner SR. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
49. Timinskas A, Butkus V, Janulaitis A, (1995). Sequence motifs characteristic for DNA (cytosine-N4) and DNA (adenine-N6) methyltransferases. Classification of all DNA methyltransferases. Gene 157: 3-11.
50. Murray K, Hughes SG, Brown JS, Bruce SA. (1976) Isolation and characterization of two sequence-specific endonucleases from Anabaena variabilis. Biochem J 159: 317-22.
51. Hughes SG, Murray K. (1980) The nucleotide sequences recognized by endonucleases AvaI and AvaII from Anabaena variabilis. Biochem. J 185: 65-75.
52. Clark TA, Lu X, Luong K, Dai Q, Boitano M, et al. (2013) Enhanced 5- methylcytosine detection in single-molecule, real-time sequencing via Tet1 oxidation. BMC Biol 22: 11:4.
53. Kozdon JB, Melfi MD, Luong K, Clark TA, Boitano M, et al. (2013) Global methylation state at base-pair resolution of the Caulobacter genome throughout the cell cycle. Proc Natl Acad Sci U S A 110: E4658-E4667.
54. Furmanek-Blaszk B, Boratynski R, Zolcinska N, Sektas M. (2009) M1.MboII and M2.MboII type IIS methyltransferases: different specificities, the same target. Microbiology 155: 1111-1121.
55. O'Driscoll J, Glynn F, Cahalane O, O'Connell-Motherway M, Fitzgerald GF, et al. (2004) Lactococcal plasmid pNP40 encodes a novel, temperature-sensitive restriction-modification system. Appl Environ Microbiol 70: 5546-5556. (Pubitemid 39279633)
56. O'Driscoll J, Fitzgerald GF, van Sinderen D. (2005) A dichotomous epigenetic mechanism governs expression of the LlaJI restriction/modification system. Mol Microbiol 57: 1532-44. (Pubitemid 41337384)
57. O'Driscoll J, Heiter DF, Wilson GG, Fitzgerald GF, Roberts R, et al. (2006) A genetic dissection of the LlaJI restriction cassette reveals insights on a novel bacteriophage resistance system. BMC Microbiol 6: 40.
58. Kaczorowski T, Sektas M, Skowron P, Podhajska AJ (1999) The FokI methyltransferase from Flavobacterium okeanokoites. Purification and characterization of the enzyme and its truncated derivatives. Mol Biotechnol 13: 1-15. (Pubitemid 30066700)
59. Sugisaki H, Yamamoto K, Takanami M (1991) The HgaI restrictionmodification system contains two cytosine methylase genes responsible for modification of different DNA strands. J Biol Chem 266: 13952-13957. (Pubitemid 21907446)
60. O'Sullivan DJ, Zagula K, Klaenhammer TR (1995) In vivo restriction by LlaI is encoded by three genes, arranged in an operon with llaIM, on the conjugative Lactococcus plasmid pTR2030. J Bacteriol 177: 134-143.
61. Hill C, Miller LA, Klaenhammer TR (1991) In vivo genetic exchange of a functional domain from a type II A methylase between lactococcal plasmid pTR2030 and a virulent bacteriophage. J Bacteriol 173(14):4363-70.
62. Bachmann BJ (1972) Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 36: 525-557.
63. De Ruyter PG, Kuipers OP, de Vos WM (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62: 3662-3667. (Pubitemid 26329592)