Comparative genomics of Bifidobacterium animalis subsp. lactis reveals a strict monophyletic bifidobacterial taxon

Applied and Environmental Microbiology

Volumn 79, Issue 14, 2013, Pages 4304-4315

  Milani, Christian ^a   Duranti, Sabrina ^a   Lugli, Gabriele Andrea ^a   Bottacini, Francesca ^b   Strati, Francesco ^a   Arioli, Stefania ^c   Foroni, Elena ^a   Turroni, Francesca ^b   van Sinderen, Douwe ^b   Ventura, Marco ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BIFIDOBACTERIUM ANIMALIS; COMPARATIVE GENOMIC; COMPARATIVE GENOMICS; FOOD INDUSTRIES; GENETIC MAKE-UP; GENETIC RELATEDNESS; GENETIC VARIABILITY; LACTIS STRAIN;

BIOTECHNOLOGY; MICROBIOLOGY;

GENES;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PROTEOME; TETRACYCLINE;

COMPARATIVE STUDY; FOOD INDUSTRY; GENETIC ANALYSIS; GENOMICS; HEALTH CARE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BIFIDOBACTERIUM; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; DNA SEQUENCE; DRUG EFFECT; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIFIDOBACTERIUM; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEOME; SEQUENCE ANALYSIS, DNA; TETRACYCLINE; TETRACYCLINE RESISTANCE;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS;

EID: 84879824186     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00984-13     Document Type: Article

References (63)

1. Chenoll E, Casinos B, Bataller E, Astals P, Echevarria J, Iglesias JR, Balbarie P, Ramon D, Genoves S. 2011. Novel probiotic Bifidobacterium bifidum CECT 7366 strain active against the pathogenic bacterium Helicobacter pylori. Appl. Environ. Microbiol. 77:1335-1343.
2. Shirasawa Y, Shibahara-Sone H, Iino T, Ishikawa F. 2010. Bifidobacterium bifidum BF-1 suppresses Helicobacter pylori-induced genes in human epithelial cells. J. Dairy Sci. 93:4526-4534.
3. Khailova L, Mount Patrick SK, Arganbright KM, Halpern MD, Kinouchi T, Dvorak B. 2010. Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 299:G1118-G1127.
4. Guglielmetti S, Mora D, Gschwender M, Popp K. 2011. Randomised clinical trial: Bifidobacterium bifidum MIMBb75 significantly alleviates irritable bowel syndrome and improves quality of life-a double-blind, placebo-controlled study. Aliment. Pharmacol. Ther. 33:1123-1132.
5. Malago JJ, Tooten PC, Koninkx JF. 2010. Anti-inflammatory properties of probiotic bacteria on Salmonella-induced IL-8 synthesis in enterocytelike Caco-2 cells. Benef. Microbes 1:121-130.
6. Ventura M, Turroni F, Motherway MO, MacSharry J, van Sinderen D. 2012. Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol. 20:467- 476.
7. 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.
8. Turroni F, van Sinderen D, Ventura M. 2011. Genomics and ecological overview of the genus Bifidobacterium. Int. J. Food Microbiol. 149:37- 44.
9. Ventura M, Canchaya C, Zhang Z, Bernini V, Fitzgerald GF, van Sinderen D. 2006. How high G+C Gram-positive bacteria and in particular bifidobacteria cope with heat stress: protein players and regulators. FEMS Microbiol. Rev. 30:734 -759.
10. Ventura M, Turroni F, van Sinderen D. 2012. Probiogenomics as a tool to obtain genetic insights into adaptation of probiotic bacteria to the human gut. Bioeng. Bugs 3:73-79.
11. Lee JH, O'Sullivan DJ. 2010. Genomic insights into bifidobacteria. Microbiol. Mol. Biol. Rev. 74:378-416.
12. Garrigues C, Johansen E, Pedersen MB. 2010. Complete genome sequence of Bifidobacterium animalis subsp. lactis BB-12, a widely consumed probiotic strain. J. Bacteriol. 192:2467-2468.
13. Bottacini F, Dal Bello F, Turroni F, Milani C, Duranti S, Foroni E, Viappiani A, Strati F, Mora D, van Sinderen D, Ventura M. 2011. Complete genome sequence of Bifidobacterium animalis subsp. lactis BLC1. J. Bacteriol. 193:6387- 6388.
14. Barrangou R, Briczinski EP, Traeger LL, Loquasto JR, Richards M, Horvath P, Coute-Monvoisin AC, Leyer G, Rendulic S, Steele JL, Broadbent JR, Oberg T, Dudley EG, Schuster S, Romero DA, Roberts RF. 2009. Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J. Bacteriol. 191:4144- 4151.
15. Kim JF, Jeong H, Yu DS, Choi SH, Hur CG, Park MS, Yoon SH, Kim DW, Ji GE, Park HS, Oh TK. 2009. Genome sequence of the probiotic bacterium Bifidobacterium animalis subsp. lactis AD011. J. Bacteriol. 191: 678-679.
16. Chervaux C, Grimaldi C, Bolotin A, Quinquis B, Legrain-Raspaud S, van Hylckama Vlieg JE, Denariaz G, Smokvina T. 2011. Genome sequence of the probiotic strain Bifidobacterium animalis subsp. lactis CNCM I-2494. J. Bacteriol. 193:5560 -5561.
17. Sun Z, Chen X, Wang J, Gao P, Zhou Z, Ren Y, Sun T, Wang L, Meng H, Chen W, Zhang H. 2010. Complete genome sequence of probiotic Bifidobacterium animalis subsp. lactis strain V9. J. Bacteriol. 192:4080- 4081.
18. Stahl B, Barrangou R. 2012. Complete genome sequences of probiotic strains Bifidobacterium animalis subsp. lactis B420 and Bi-07. J. Bacteriol. 194:4131- 4132.
19. Ventura M, Reniero R, Zink R. 2001. Specific identification and targeted characterization of Bifidobacterium lactis from different environmental isolates by a combined multiplex-PCR approach. Appl. Environ. Microbiol. 67:2760 -2765.
20. Ventura M, Zink R. 2003. Comparative sequence analysis of the tuf and recA genes and restriction fragment length polymorphism of the internal transcribed spacer region sequences supply additional tools for discriminating Bifidobacterium lactis from Bifidobacterium animalis. Appl. Environ. Microbiol. 69:7517-7522.
21. Briczinski EP, Loquasto JR, Barrangou R, Dudley EG, Roberts AM, Roberts RF. 2009. Strain-specific genotyping of Bifidobacterium animalis subsp. lactis by using single-nucleotide polymorphisms, insertions, and deletions. Appl. Environ. Microbiol. 75:7501-7508.
22. International Organization for Standardization. 2010. ISO 10932:2010 (IDF 223:2010). Milk and milk products-determination of the minimal inhibitory concentration (MIC) of antibiotics applicable to bifidobacteria and non-enterococcal lactic acid bacteria (LAB). International Organization for Standardization, Geneva, Switzerland.
23. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WE, Wetter T, Suhai S. 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14:1147-1159.
24. Gish W, States DJ. 1993. Identification of protein coding regions by database similarity search. Nat. Genet. 3:266 -272.
25. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944 -945.
26. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119.
27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403- 410.
28. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
29. Roberts RJ, Vincze T, Posfai J, Macelis D. 2010. REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res. 38:D234-D236.
30. Busch W, Saier MH, Jr. 2002. The transporter classification (TC) system, 2002. Crit. Rev. Biochem. Mol. Biol. 37:287-337.
31. Loquasto JR, Barrangou R, Dudley EG, Roberts RF. 2011. Short communication: the complete genome sequence of Bifidobacterium animalis subspecies animalis ATCC 25527(T) and comparative analysis of growth in milk with B. animalis subspecies lactis DSM 10140(T). J. Dairy Sci. 94:5864 -5870.
32. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M, Pridmore RD, Arigoni F. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. U. S. A. 99:14422-14427.
33. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB, Price NP, Richardson PM, Mills DA. 2008. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. U. S. A. 105:18964 -18969.
34. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sanchez B, Bidossi A, Ferrarini A, Giubellini V, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Fitzgerald GF, Mills D, Margolles A, Kelly D, van Sinderen D, Ventura M. 2010. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc. Natl. Acad. Sci. U. S. A. 107:19514 -19519.
35. Ventura M, Turroni F, Zomer A, Foroni E, Giubellini V, Bottacini F, Canchaya C, Claesson MJ, He F, Mantzourani M, Mulas L, Ferrarini A, Gao B, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Gupta RS, Zhang Z, Beighton D, Fitzgerald GF, O'toole PW, van Sinderen D. 2009. The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet. 5:e1000785.
36. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O'Brien F, Flynn K, Casey PG, 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 hostcolonization factor. Proc. Natl. Acad. Sci. U. S. A. 108:11217-11222.
37. Pearson WR. 2000. Flexible sequence similarity searching with the FASTA3 program package. Methods Mol. Biol. 132:185-219.
38. van Dongen S. 2000. Graph clustering by flow simulation. Ph.D. thesis. University of Utrecht, Utrecht, The Netherlands.
39. Thompson JD, Gibson TJ, Higgins DG. 2002. Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics 2002: 2.3.1-2.3.22.
40. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696- 704.
41. Darling AE, Mau B, Perna NT. 2010. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147.
42. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374 -378.
43. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649.
44. Zhao Y, Wu J, Yang J, Sun S, Xiao J, Yu J. 2012. PGAP: pan-genomes analysis pipeline. Bioinformatics 28:416-418.
45. Tettelin H, Riley D, Cattuto C, Medini D. 2008. Comparative genomics: the bacterial pan-genome. Curr. Opin. Microbiol. 11:472- 477.
46. Gueimonde M, Florez AB, van Hoek AH, Stuer-Lauridsen B, Stroman P, de los Reyes-Gavilan CG, Margolles A. 2010. Genetic basis of tetracycline resistance in Bifidobacterium animalis subsp. lactis. Appl. Environ. Microbiol. 76:3364 -3369.
47. Ammor MS, Florez AB, Alvarez-Martin P, Margolles A, Mayo B. 2008. Analysis of tetracycline resistance tet(W) genes and their flanking sequences in intestinal Bifidobacterium species. J. Antimicrob. Chemother. 62:688-693.
48. Flórez AB, Ammor MS, Alvarez-Martin P, Margolles A, Mayo B. 2006. Molecular analysis of tet(W) gene-mediated tetracycline resistance in dominant intestinal Bifidobacterium species from healthy humans. Appl. Environ. Microbiol. 72:7377-7379.
49. Lee JH, Karamychev VN, Kozyavkin SA, Mills D, Pavlov AR, Pavlova NV, Polouchine NN, Richardson PM, Shakhova VV, Slesarev AI, Weimer B, O'Sullivan DJ. 2008. Comparative genomic analysis of the gut bacterium Bifidobacterium longum reveals loci susceptible to deletion during pure culture growth. BMC Genomics 9:247.
50. Scott KP, Barbosa TM, Forbes KJ, Flint HJ. 1997. High-frequency transfer of a naturally occurring chromosomal tetracycline resistance element in the ruminal anaerobe Butyrivibrio fibrisolvens. Appl. Environ. Microbiol. 63:3405-3411.
51. Burdett V. 1993. tRNA modification activity is necessary for Tet(M)- mediated tetracycline resistance. J. Bacteriol. 175:7209 -7215.
52. Henz SR, Huson DH, Auch AF, Nieselt-Struwe K, Schuster SC. 2005. Whole-genome prokaryotic phylogeny. Bioinformatics 21:2329 -2335.
53. Chan CX, Beiko RG, Ragan MA. 2006. Detecting recombination in evolving nucleotide sequences. BMC Bioinformatics 7:412. doi:10.1186 /1471-2105-7-412.
54. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D. 2007. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 71:495- 548.
55. Bottacini F, Medini D, Pavesi A, Turroni F, Foroni E, Riley D, Giubellini V, Tettelin H, van Sinderen D, Ventura M. 2010. Comparative genomics of the genus Bifidobacterium. Microbiology 156:3243-3254.
56. Ventura M, Canchaya C, Fitzgerald GF, Gupta RS, van Sinderen D. 2007. Genomics as a means to understand bacterial phylogeny and ecological adaptation: the case of bifidobacteria. Antonie Van Leeuwenhoek 91:351-372.
57. 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.
58. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709-1712.
59. Jansen R, Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565-1575.
60. Mojica FJ, Diez-Villasenor C, Soria E, Juez G. 2000. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol. Microbiol. 36:244 -246.
61. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV. 2006. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1:7.
62. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. 2005. The microbial pan-genome. Curr. Opin. Genet. Dev. 15:589 -594.
63. Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, Wernegreen JJ, Sandstrom JP, Moran NA, Andersson SG. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.