Evaluation of genetic diversity among strains of the human gut commensal Bifidobacterium adolescentis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Duranti, Sabrina ^a   Milani, Christian ^a   Lugli, Gabriele Andrea ^a   Mancabelli, Leonardo ^a   Turroni, Francesca ^a   Ferrario, Chiara ^a   Mangifesta, Marta ^b   Viappiani, Alice ^b   Sanchez, Borja ^c,e   Margolles, Abelardo ^c   Van Sinderen, Douwe ^d   Ventura, Marco ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b Italy   (Italy)

^c CSIC   (Spain)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e UNIVERSITY OF VIGO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CARBOHYDRATE; POLYSACCHARIDE;

ANIMAL; BACTERIAL GENOME; BIFIDOBACTERIUM ADOLESCENTIS; BOVINE; CHEMISTRY; DIET; FECES; GENETIC VARIATION; GENETICS; GENOMICS; HUMAN; INTESTINE; INTESTINE FLORA; ISOLATION AND PURIFICATION; MICROBIOLOGY; MILK; OPEN READING FRAME; RUMEN;

ANIMALS; BIFIDOBACTERIUM ADOLESCENTIS; CARBOHYDRATES; CATTLE; DIET; DNA, BACTERIAL; FECES; GASTROINTESTINAL MICROBIOME; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; HUMANS; INTESTINES; MILK; OPEN READING FRAMES; POLYSACCHARIDES; RUMEN;

EID: 84963652891     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23971     Document Type: Article

References (59)

1. Turroni, F. et al. Diversity of bifidobacteria within the infant gut microbiota. Plos One 7, e36957, doi: 10.1371/journal.pone.0036957 (2012).
2. Turroni, F. et al. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 75, 1534-1545, doi: 10.1128/AEM.02216-08 (2009).
3. Ventura, M. et al. From bacterial genome to functionality; case bifidobacteria. Int J Food Microbiol 120, 2-12, doi: 10.1016/j. ijfoodmicro.2007.06.011 (2007).
4. Ventura, M. et al. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71, 495-548, doi: 10.1128/MMBR.00005-07 (2007).
5. Milani, C. et al. Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl Environ Microbiol 80, 6290-6302, doi: 10.1128/AEM.02308-14 (2014).
6. Lugli, G. A. et al. Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics. Appl Environ Microbiol 80, 6383-6394, doi: 10.1128/AEM.02004-14 (2014).
7. Turroni, F., van Sinderen, D., Ventura, M. Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 149, 37-44, doi: 10.1016/j.ijfoodmicro.2010.12.010 (2011).
8. Duranti, S. et al. Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22L. Appl Environ Microbiol 80, 6080-6090, doi: 10.1128/AEM.01993-14 (2014).
9. Duranti, S. et al. Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ Microbiol 17, 2515-2531, doi: 10.1111/1462-2920.12743 (2015).
10. Bottacini, F. et al. Comparative genomics of the Bifidobacterium breve taxon. BMC genomics 15, 170, doi: 10.1186/1471-2164-15-170 (2014).
11. Turroni, F. et al. Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions. Proc Natl Acad Sci USA 110, 11151-11156, doi: 10.1073/pnas.1303897110 (2013).
12. Turroni, F. et al. Expression of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in response to environmental gut conditions. FEMS Microbiol Lett 357, 23-33, doi: 10.1111/1574-6968.12509 (2014).
13. O'Connell Motherway, M. et al. 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 USA 108, 11217-11222, doi: 10.1073/pnas.1105380108 (2011).
14. Foroni, E. et al. Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microb Cell Fact 10 Suppl 1, S16, doi: 10.1186/1475-2859-10-S1-S16 (2011).
15. Turroni, F. et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA 107, 19514-19519, doi: 10.1073/pnas.1011100107 (2010).
16. Turroni, F., Milani, C., van Sinderen, D., Ventura, M. Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: an example of possible human-microbe co-evolution. Gut microbes 2, 183-189 (2011).
17. Dyachkova, M. S. et al. Draft Genome Sequences of Bifidobacterium angulatum GT102 and Bifidobacterium adolescentis 150: Focusing on the Genes Potentially Involved in the Gut-Brain Axis. Genome Announc 3, doi: 10.1128/genomeA.00709-15 (2015).
18. Killer, J., Sedlacek, I., Rada, V., Havlik, J., Kopecny, J. Reclassification of Bifidobacterium stercoris Kim et al. 2010 as a later heterotypic synonym of Bifidobacterium adolescentis. Int J Syst Evol Micr 63, 4350-4353, doi: 10.1099/ijs.0.054957-0 (2013).
19. O'Callaghan, A., Bottacini, F., O'Connell Motherway, M., van Sinderen, D. Pangenome analysis of Bifidobacterium longum and site-directed mutagenesis through by-pass of restriction-modification systems. BMC genomics 16, 832, doi: 10.1186/s12864-015-1968-4 (2015).
20. Milani, C. et al. Comparative genomics of Bifidobacterium animalis subsp. lactis reveals a strict monophyletic bifidobacterial taxon. Appl Environ Microbiol 79, 4304-4315, doi: 10.1128/AEM.00984-13 (2013).
21. Powell, S. et al. eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acid Res 42, D231-D239, doi: 10.1093/nar/gkt1253 (2014).
22. Milani, C. et al. Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci Rep. 5, 15782, doi: 10.1038/srep15782 (2015).
23. Tettelin, H. et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial 'pangenome' (vol 102, pg 13950, 2005). Proc Natl Acad Sci USA 102, 16530-16530, doi: 10.1073/pnas.0508532102 (2005).
24. Duranti, S. et al. Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ Microbiol 17, 2515-2531, doi: 10.1111/1462-2920.12743 (2015).
25. Richter, M., Rossello-Mora, R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106, 19126-19131, doi: 10.1073/pnas.0906412106 (2009).
26. Waack, S. et al. Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models. BMC bioinformatics 7, Artn 142 doi:10.1186/1471-2105-7-142 (2006).
27. Podell, S., Gaasterland, T. DarkHorse: a method for genome-wide prediction of horizontal gene transfer. Genome Biol 8, Artn R16, doi: 10.1186/Gb-2007-8-2-R16 (2007).
28. Imam, S., Chen, Z., Roos, D. S., Pohlschroder, M. Identification of surprisingly diverse type IV pili, across a broad range of grampositive bacteria. Plos One 6, e28919, doi: 10.1371/journal.pone.0028919 (2011).
29. Bottacini, F. et al. Discovery of a conjugative megaplasmid in Bifidobacterium breve. Appl Environ Microbiol 81, 166-176, doi: 10.1128/AEM.02871-14 (2015).
30. Dominguez, W., O'Sullivan, D. J. Developing an efficient and reproducible conjugation-based gene transfer system for bifidobacteria. Microbiol-Sgm 159, 328-338, doi: 10.1099/mic.0.061408-0 (2013).
31. Ventura, M. et al. Prophage-like elements in bifidobacteria: insights from genomics, transcription, integration, distribution, and phylogenetic analysis. Appl Environ Microbiol 71, 8692-8705, doi: 10.1128/AEM.71.12.8692-8705.2005 (2005).
32. Ventura, M. et al. Comparative analyses of prophage-like elements present in bifidobacterial genomes. Appl Environ Microbiol 75, 6929-6936, doi: 10.1128/AEM.01112-09 (2009).
33. Lugli, G. A. et al. Prophages of the genus Bifidobacterium as modulating agents of the infant gut microbiota. Environ Microbiol doi: 10.1111/1462-2920.13154 (2015).
34. Turroni, F. et al. Analysis of predicted carbohydrate transport systems encoded by Bifidobacterium bifidum PRL2010. Appl Environ Microbiol 78, 5002-5012, doi: 10.1128/AEM.00629-12 (2012).
35. Pokusaeva, K., Fitzgerald, G. F., van Sinderen, D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6, 285-306, doi: 10.1007/s12263-010-0206-6 (2011).
36. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acid Res 42, D490-495, doi: 10.1093/nar/gkt1178 (2014).
37. van der Maarel, M. J., van der Veen, B., Uitdehaag, J. C., Leemhuis, H., Dijkhuizen, L. Properties and applications of starchconverting enzymes of the alpha-amylase family. J Biotechnol 94, 137-155 (2002).
38. Ye, Y. B., Wei, B., Wen, L., Rayner, S. BlastGraph: a comparative genomics tool based on BLAST and graph algorithms. Bioinformatics 29, 3222-3224, doi: 10.1093/bioinformatics/btt553 (2013).
39. Farris, J. S. Phylogenetic Analysis Under Dollo's Law. Syst Zool 26, 77-78 (1977).
40. Sela, D. A. et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci USA 105, 18964-18969, doi: 10.1073/pnas.0809584105 (2008).
41. Ruiz-Moyano, S. et al. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol 79, 6040-6049, doi: 10.1128/AEM.01843-13 (2013).
42. Ventura, M., Reniero, R., Zink, R. Specific identification and targeted characterization of Bifidobacterium lactis from different environmental isolates by a combined multiplex-PCR approach. Appl Environ Microbiol 67, 2760-2765, doi: 10.1128/AEM.67.6.2760-2765.2001 (2001).
43. Sambrook, J., David W. Russell. Molecular cloning a laboratory manual. (Cold Spring Harbor Laboratory Press, 2001).
44. Lugli, G. A., Milani, C., Mancabelli, L., van Sinderen, D., Ventura, M. MEGAnnotator: a user-friendly pipeline for microbial genomes assembly and annotation. FEMS Microbial Lett. doi: 10.1093/femsle/fnw049 (2016).
45. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC bioinformatics 11, 119, doi: 10.1186/1471-2105-11-119 (2010).
46. Gish, W., States, D. J. Identification of protein coding regions by database similarity search. Nat Genet 3, 266-272, doi: 10.1038/ng0393-266 (1993).
47. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., Lipman, D. J. Basic local alignment search tool. J Mol Biol 215, 403-410, doi: 10.1016/S0022-2836(05)80360-2 (1990).
48. Rutherford, K. et al. Artemis: sequence visualization and annotation. Bioinformatics 16, 944-945 (2000).
49. Lowe, T. M., Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acid Res 25, 955-964 (1997).
50. Roberts, R. J., Vincze, T., Posfai, J., Macelis, D. REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acid Res 43, D298-299, doi: 10.1093/nar/gku1046 (2015).
51. Busch, W., Saier, M. H. The Transporter Classification (TC) system, 2002. Crit Rev Biochem Mol 37, 287-337, doi: 10.1080/10409230290771528 (2002).
52. Schmid, R., Blaxter, M. L. annot8r: GO, EC and KEGG annotation of EST datasets. BMC bioinformatics 9, Artn 180, doi: 10.1186/1471-2105-9-180 (2008).
53. Gao, F., Zhang, C. T. GC-Profile: a web-based tool for visualizing and analyzing the variation of GC content in genomic sequences. Nucleic Acid Res 34, W686-W691, doi: 10.1093/nar/gkl040 (2006).
54. McInerney, J. O. G. C. U. A.: General codon usage analysis. Bioinformatics 14, 372-373, doi: 10.1093/bioinformatics/14.4.372 (1998).
55. Pearson, W. R. Flexible sequence similarity searching with the FASTA3 program package. Methods Mol Biol 132, 185-219 (2000).
56. van Dongen, S. Graph clustering by flow simulation. PhD thesis, University of Utrecht, The Netherlands (2000).
57. Thompson, J. D., Gibson, T. J., Higgins, D. G. Multiple sequence alignment using ClustalW and ClustalX. Current protocols in bioinformatics Chapter 2, Unit 2 3, doi: 10.1002/0471250953.bi0203s00 (2002).
58. Guindon, S., Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696-704 (2003).
59. Zhao, Y. et al. PGAP: pan-genomes analysis pipeline. Bioinformatics 28, 416-418, doi: 10.1093/bioinformatics/btr655 (2012).