Genome-scale analyses of health-promoting bacteria: Probiogenomics

Nature Reviews Microbiology

Volumn 7, Issue 1, 2009, Pages 61-71

  Ventura, Marco ^a   O'Flaherty, Sarah ^b   Claesson, Marcus J ^c   Turroni, Francesca ^a   Klaenhammer, Todd R ^b   van Sinderen, Douwe ^c   O'Toole, Paul W ^c  

^a UNIVERSITY OF PARMA   (Italy)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

PREBIOTIC AGENT; PROBIOTIC AGENT; TRANSCRIPTOME;

BACTERIAL GENETICS; BACTERIAL GENOME; BACTEROIDES THETAIOTAOMICRON; BIFIDOBACTERIUM; COMMENSAL; DIET SUPPLEMENTATION; EVOLUTIONARY ADAPTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENOMICS; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS HELVETICUS; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; MOLECULAR GENETICS; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROBIOGENOMICS; REVIEW;

BIFIDOBACTERIUM; LACTOBACILLUS;

EID: 57649184474     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2047     Document Type: Review

References (92)

1. Backhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. & Gordon, J. I. Host-bacterial mutualism in the human intestine. Science 307 1915-1920 (2005).
2. Eckburg, P. B. et al. Diversity of the human intestinal microbial flora. Science 308, 1635-1638 (2005).
3. Seksik, P. et al. Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52 237-242 (2003).
4. Turroni, F., Ribbera, A., Foroni, E., van Sinderen, D. & Ventura, M. Human gut microbiota and bifidobacteria: From composition to functionality. Antonie Van Leeuwenhoek 94, 35-50 (2008).
5. Rajilic-Stojanovic, M., Smidt, H. & de Vos, W. M. Diversity of the human gastrointestinal tract microbiota revisited. Environ. Microbiol. 9, 2125-2136 (2007).
6. Ley, R. E., Peterson, D. A. & Gordon, J. I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837-848 (2006).
7. Guarner, F. & Malagelada, J. R. Gut flora in health and disease. Lancet 361, 512-519 (2003).
8. Hooper, L. V. & Gordon, J. I. Commensal host-bacterial relationships in the gut. Science 292, 1115-1118 (2001).
9. Backhed, F. et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl Acad. Sci. USA 101, 15718-15723 (2004).
10. Samuel, B. S. & Gordon, J. I. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc. Natl Acad. Sci. USA 103, 10011-10016 (2006).
11. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031 (2006).
12. Frank, D. N. et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl Acad. Sci. USA 104, 13780-13785 (2007).
13. Kassinen, A. et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133, 24-33 (2007).
14. Manichanh, C. et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55, 205-211 (2006).
15. Food and Agriculture Organization of the United Nations and World Health Organization. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. (FAO/WHO, Cordoba, Argentina, 2001).
16. Marco, M. L., Pavan, S. & Kleerebezem, M. Towards understanding molecular modes of probiotic action. Curr. Opin. Biotechnol. 17 204-210 (2006).
17. O'Hara, A. M. & Shanahan, F. Mechanisms of action of probiotics in intestinal diseases. Scientific World J. 7, 31-46 (2007).
18. Saxelin, M., Tynkkynen, S., Mattila-Sandholm, T. & de Vos, W. M. Probiotic and other functional microbes: From markets to mechanisms. Curr. Opin. Biotechnol. 16, 204-211 (2005).
19. Ventura, M. et al. Genomics of Actinobacteria: Tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 71, 495-548 (2007).
20. Joyce, A. R. & Palsson, B. O. The model organism as a system: integrating 'omics' data sets. Nature Rev. Mol. Cell Biol. 7 198-210 (2006).
21. Ventura, M. et al. Analysis of bifidobacterial evolution using a multilocus approach. Int. J. Syst. Evol. Microbiol. 56, 2783-2792 (2006).
22. Tissier, M. H. Recherche Sur La Flore Intestinale Des Nourissons (Etat Normal Et Pathologique). Thesis, Univ. Paris, France (1906).
23. Ventura, M., Canchaya, C., Fitzgerald, G. F., Gupta, R. S. & van Sinderen, D. Genomics as a means to understand bacterial phylogeny and ecological adaptation: The case of bifidobacteria. Antonie Van Leeuwenhoek 91, 351-372 (2007).
24. Schell, M. A. et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl Acad. Sci. USA 99, 14422-14427 (2002).
25. Gibson, G. R. & Roberfroid, M. B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 125, 1401-1412 (1995).
26. Flint, H. J., Bayer, E. A., Rincon, M. T, Lamed, R. & White, B. A. Polysaccharide utilization by gut bacteria: Potential for new insights from genomic analysis. Nature Rev. Microbiol. 6, 121-131 (2008).
27. Sonnenburg, J. L. et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955-1959 (2005).
28. Hooper, L. V., Xu, J., Falk, P. G., Midtvedt, T. & Gordon, J. I. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc. Natl Acad. Sci. USA 96, 9833-9838 (1999).
29. Hinz, S. W., Verhoef, R., Schols, H. A., Vincken, J. P. & Voragen, A. G. Type I arabinogalactan contains β-D-Galp-(1 → 3 -β-D-Galp structural elements. Carbohydr. Res. 340, 2135-2143 (2005).
30. Ryan, S. M., Fitzgerald, G. F. & van Sinderen, D. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl. Environ. Microbiol. 72, 5289-5296 (2006).
31. Maze, A., O'Connell-Motherway, M., Fitzgerald, G. F., Deutscher, J. & van Sinderen, D. Identification and characterization of a fructose phosphotransferase system in Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 73, 545-553 (2007).
32. van den Broek, L. A., Hinz, S. W., Beldman, G., Vincken, J. P. & Varagen, A. G. Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol. Nutr. Food Res. 52, 146-163 (2008).
33. Siezen, R. et al. Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific Gram-positive bacteria. BMC Genomics 7 126 (2006).
34. Hooper, L. V., Midtvedt, T. & Gordon, J. I. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22, 283-307 (2002).
35. Hoskins, L. C. et al. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J. Clin. Invest. 75, 944-953 (1985).
36. Ruas-Madiedo, P., Gueimonde, M., Fernandez-Garcia, M., de los Reyes-Gavilan, C. G. & Margolles, A. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl. Environ. Microbiol. 74, 1936-1940 (2008).
37. Ventura, M., van Sinderen, D., Fitzgerald, G. F. & Zink, R. Insights into the taxonomy, genetics and physiology of bifidobacteria. Antonie Van Leeuwenhoek 86, 205-223 (2004).
38. Ehrmann, M. A., Korakli, M. & Vogel, R. F. Identification of the gene for β-fructofuranosidase of Bifidobacterium lactis DSM 10140[T] and characterization of the enzyme expressed in Escherichia coli. Curr. Microbiol. 46, 391-397 (2003).
39. Katayama, T. et al. Molecular cloning and characterization of Bifidobacterium bifidum 1,2-α-L- fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J. Bacteriol. 186, 4885-4893 (2004).
40. Ryan, S. M., Fitzgerald, G. F. & van Sinderen, D. Transcriptional regulation and characterization of a novel β-fructofuranosidase-encoding gene from Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 71, 3475-3482 (2005).
41. Gonzalez, R., Klaassens, E. S., Malinen, E., de Vos, W. M. & Vaughan. E. E. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk and galactooligosaccharide. Appl. Environ. Microbiol. 74, 4686-4694 (2008)..
42. Liepke, C. et al. Human milk provides peptides highly stimulating the growth of bifidobacteria. Eur. J. Biochem. 269, 712-718 (2002).
43. Ivanov, D. et al. A serpin from the gut bacterium Bifidobacterium longum inhibits eukaryotic elastase-like serine proteases. J. Biol. Chem. 281, 17246-17252 (2006).
44. Potempa, J., Korzus, E. & Travis, J. The serpin superfamily of proteinase inhibitors: Structure, function, and regulation. J. Biol. Chem. 269, 15957-15960 (1994).
45. Sonnenhurg, J. L., Chen, C. T. & Gordon, J. I. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol. 4, e413 (2006).
46. Kato, S., Haruta, S., Cui, Z. J., Ishii, M. & Igarashi, Y. Stable coexistence of five bacterial strains as a cellulose-degrading community. Appl. Environ. Microbiol. 71, 7099-7106 (2005).
47. Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712 (2007).
48. Klijn, A., Mercenier, A. & Arigoni, F. Lessons from the genomes of bifidobacteria. FEMS Microbiol. Rev. 29, 491-509 (2005).
49. Aas, J. A. et al. Bacteria of dental caries in primary and permanent teeth in children and young adults. J. Clin. Microbiol. 46, 1407-1417 (2008).
50. Makarova, K. S. & Koonin, E. V. Evolutionary genomics of lactic acid bacteria. J. Bacteriol. 189, 1199-1208 (2007).
51. Claesson, M. J. et al. Multireplicon genome architecture of Lactobacillus salivarius. Proc. Natl Acad. Sci. USA 103, 6718-6723 (2006).
52. Pfeiler, E. A. & Klaenhammer, T. R. The genomics of lactic acid bacteria. Trends Microbiol. 15, 546-553 (2007).
53. van de Guchte, M. et al. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc. Natl Acad. Sci. USA 103, 9274-9279 (2006).
54. Callanan, M. et al. Genome sequence of Lactobacillus helveticus an organism distinguished by selective gene loss and insertion sequence element expansion. J. Bacteriol. 190, 727-735 (2008).
55. Altermann, E. et al. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl Acad. Sci. USA 102, 3906-3912 (2005).
56. Walter, J. et al. Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl. Environ. Microbiol. 69, 2044-2051 (2003).
57. Bron, P. A., Grangette, C., Mercenier, A., de Vos, W. M. & Kleerebezem, M. Identification of Lactobacillus plantarum genes that are induced in the gastrointestinal tract of mice. J. Bacteriol. 186, 5721-5729 (2004).
58. Oozeer, R. et al. Differential activities of four Lactobacillus casei promoters during bacterial transit through the gastrointestinal tracts of human-microbiota-associated mice. Appl. Environ. Microbiol. 71, 1356-1363 (2005).
59. Denou, E. et al. Gene expression of commensal Lactobacillus johnsonii strain NCC533 during in vitro growth and in the murine gut. J. Bacteriol. 189, 8109-8119 (2007).
60. Denou, E. et al. Identification of genes associated with the long-gut-persistence phenotype of the probiotic Lactobacillus johnsonii strain NCC533 using a combination of genomics and transcriptome analysis. J. Bacteriol. 190, 3161-3168 (2008).
61. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: The unseen majority. Proc. Natl Acad. Sci. USA 95, 6578-6583 (1998).
62. Tannock, G. W. et al. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl. Environ. Microbiol. 66, 2578-2588 (2000).
63. Martin, F. P. et al. Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Mol. Syst. Biol. 4, 157 (2008).
64. Hickson, M. et al. Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: Randomised double blind placebo controlled trial. Brit. Med. J. 335, 80 (2007).
65. Sullivan, A. & Nord., C. E. Probiotics and gastrointestinal diseases. J. Intern. Med. 257, 78-92 (2005).
66. Kelly, M. C., Mequio, M. J. & Pybus, V. Inhibition of vaginal lactobacilli by a bacteriocin-like inhibitor produced by Enterococcus faecium 62-66: Potential significance for bacterial vaginosis. Infect. Dis. Obstet. Gynecol. 11, 147-156 (2003).
67. Corr, S. C. et al. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc. Natl Acad. Sci. USA 104, 7617-7621 (2007).
68. Casey, P. G. et al. A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 73, 1858-1863 (2007).
69. Makarova, K. et al. Comparative genomics of the lactic acid bacteria. Proc. Natl Acad. Sci. USA 103, 15611-15616 (2006).
70. Kleerebezem, M. et al. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl Acad. Sci. USA 100 1990-1995 (2003).
71. Pridmore, R. D. et al. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc. Natl Acad. Sci. USA 101, 2512-2517 (2004).
72. Talarico, T. L., Casas, I. A., Chung, T. C. & Dobrogosz, W. J. Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 32, 1854-1858 (1988).
73. Santos, F. et al. The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. Microbiology 154, 81-93 (2008).
74. Sriramulu, D. D. et al. Lactobacillus reuteri DSM 20016 produces cobalamin-dependent diol dehydratase in metabolosomes and metabolizes 1,2-propanediol by disproportionation. J. Bacteriol. 190, 4559-4567 (2008).
75. Morita, H. et al. Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res. 15, 151-161 (2008).
76. Euzeby, J. P. List of bacterial names with standing in nomenclature: A folder available on the internet. Int. J. Syst. Bacteriol. 47 590-592 (1997).
77. Boekhorst, J. et al. The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. Microbiology 150, 3601-3611 (2004).
78. Berger, B. et al. Similarity and differences in the Lactobacillus acidophilus group identified by polyphasic analysis and comparative genomics. J. Bacteriol. 189, 1311-1321 (2007).
79. Nicolas, P., Bessieres, P., Ehrlich, S. D., Maguin, E. & van de Guchte, M. Extensive horizontal transfer of core genome genes between two Lactobacillus species found in the gastrointestinal tract. BMC Evol. Biol. 7, 141 (2007).
80. Klaenhammer, T. R., Barrangou, R., Buck, B. L., Azcarate-Peril, M. A. & Altermann, E. Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol. Rev. 29, 393-409 (2005).
81. Canchaya, C., Claesson, M. J., Fitzgerald, G. F., van Sinderen, D. & O'Toole, P. W. Diversity of the genus Lactobacillus revealed by comparative genomics of five species. Microbiology 152, 3185-3196 (2006).
82. Makarova, K. et al. Comparative genomics of the lactic acid bacteria. Proc. Natl Acad. Sci. USA 103, 15611-15616 (2006).
83. Claesson M. J., von Sinderen, D. & O'Toole, P. W. Lactobacillus phylogenomics - towards a reclassification of the genus. Int. J. Sys. Evo. Microbiol. (in press).
84. Teuber, M., Meile, L. & Schwarz, F. Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76, 115-137 (1999).
85. Koonin, E. V., Makarova, K. S. & Aravind, L. Horizontal gene transfer in prokaryotes: Quantification and classification. Annu. Rev. Microbiol. 55, 709-742 (2001).
86. Lloyd, A. L., Rasko, D. A. & Mobley, H. L. Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J. Bacteriol. 189, 3532-3546 (2007).
87. Pretzer, G. et al. Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J. Bacteriol. 187, 6128-6136 (2005).
88. Grangette, C. et al. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc. Natl Acad. Sci. USA 102, 10321-10326 (2005).
89. Turnbaugh, P. J. et al. The human microbiome project. Nature 449, 804-810 (2007).
90. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647-1651 (2008).
91. Lee, J. H. et al. Comparative genomic analysis of the gut bacterium Bifidobacterium longum reveals loci susceptible to deletion during pure culture growth. BMC Genomics 9, 247 (2008).
92. Leahy, S. C., Higgins, D. G., Fitzgerald, G. F. & van Sinderen, D. Getting better with bifidobacteria. J. Appl. Microbiol. 98, 1303-1315 (2005).