Glycan Utilization and Cross-Feeding Activities by Bifidobacteria

Trends in Microbiology

Volumn 26, Issue 4, 2018, Pages 339-350

  Turroni, Francesca ^a   Milani, Christian ^a   Duranti, Sabrina ^a   Mahony, Jennifer ^b   van Sinderen, Douwe ^b   Ventura, Marco ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Bifidobacterium; genomics; gut microbiota; metagenomics; probiotics

Indexed keywords

GLYCAN; POLYSACCHARIDE; PROBIOTIC AGENT;

BACTERIAL COLONIZATION; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM CROSS FEEDING; BIFIDOBACTERIUM; BIFIDOBACTERIUM ADOLESCENTIS; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM CATENULATUM; BIFIDOBACTERIUM LONGUM SUBSP. INFANTIS; CARBOHYDRATE METABOLISM; CHROMOSOME; COMMENSAL; EVOLUTIONARY ADAPTATION; GENE STRUCTURE; GLYCAN UTILIZATION; INTESTINE FLORA; NONHUMAN; PRIORITY JOURNAL; REVIEW; VERTICAL TRANSMISSION; ADAPTATION; ECOLOGY; EVOLUTION; GASTROINTESTINAL TRACT; GENETICS; HUMAN; METABOLISM; METAGENOMICS; MICROBIOLOGY; PHYSIOLOGY;

ADAPTATION, BIOLOGICAL; BIFIDOBACTERIUM; BIOLOGICAL EVOLUTION; CARBOHYDRATE METABOLISM; ECOLOGY; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; GENOME, BACTERIAL; HUMANS; METAGENOMICS; POLYSACCHARIDES; PROBIOTICS;

EID: 85032355151     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2017.10.001     Document Type: Review

References (84)

1. Milani, C., et al. Unveiling bifidobacterial biogeography across the mammalian branch of the tree of life. ISME J., 2017, 10.1038/ismej.2017.138 Published online August 22, 2017.
2. Turroni, F., et al. Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell. Mol. Life Sci. 71 (2014), 183–203.
3. Milani, C., et al. Exploring vertical transmission of bifidobacteria from mother to child. Appl. Environ. Microbiol. 81 (2015), 7078–7087.
4. Duranti, S., et al. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission. Microbiome, 5, 2017, 66.
5. Turroni, F., et al. Diversity of bifidobacteria within the infant gut microbiota. PLoS One, 7, 2012, e36957.
6. Duranti, S., et al. Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22L. Appl. Environ. Microbiol. 80 (2014), 6080–6090.
7. Duranti, S., et al. Evaluation of genetic diversity among strains of the human gut commensal Bifidobacterium adolescentis. Sci. Rep., 6, 2016, 23971.
8. Martin, R., et al. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl. Environ. Microbiol. 75 (2009), 965–969.
9. Jost, T., et al. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ. Microbiol. 16 (2014), 2891–2904.
10. O'Sullivan, A., et al. The influence of early infant-feeding practices on the intestinal microbiome and body composition in infants. Nutr. Metab. Insights 8:Suppl. 1 (2015), 1–9.
11. Fernandez, L., et al. The human milk microbiota: origin and potential roles in health and disease. Pharmacol. Res. 69 (2013), 1–10.
12. Rodriguez, J.M., The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation?. Adv. Nutr. 5 (2014), 779–784.
13. 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. U. S. A. 105 (2008), 18964–18969.
14. Turroni, F., et al. Analysis of predicted carbohydrate transport systems encoded by Bifidobacterium bifidum PRL2010. Appl. Environ. Microbiol. 78 (2012), 5002–5012.
15. Egan, M., et al. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol., 14, 2014, 282.
16. Egan, M., et al. Metabolism of sialic acid by Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 80 (2014), 4414–4426.
17. Turroni, F., et al. Glycan cross-feeding activities between bifidobacteria under in vitro conditions. Front. Microbiol., 6, 2015, 1030.
18. Turroni, F., et al. Deciphering bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach. ISME J. 10 (2016), 1656–1668.
19. Schink, B., Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81 (2002), 257–261.
20. Morris, B.E., et al. Microbial syntrophy: interaction for the common good. FEMS Microbiol. Rev. 37 (2013), 384–406.
21. Heinken, A., Thiele, I., Anoxic conditions promote species-specific mutualism between gut microbes in silico. Appl. Environ. Microbiol. 81 (2015), 4049–4061.
22. Lim, E.S., et al. The Bacterial microbiome and virome milestones of infant development. Trends Microbiol. 24 (2016), 801–810.
23. Arboleya, S., et al. Gut bifidobacteria populations in human health and aging. Front. Microbiol., 7, 2016, 1204.
24. Arboleya, S., et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J. Pediatr. 166 (2015), 538–544.
25. Schell, M.A., et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 14422–14427.
26. Milani, C., et al. Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl. Environ. Microbiol. 80 (2014), 6290–6302.
27. Milani, C., et al. Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci. Rep., 5, 2015, 15782.
28. Milani, C., et al. Genomics of the genus Bifidobacterium reveals species-specific adaptation to the glycan-rich gut environment. Appl. Environ. Microbiol. 82 (2016), 980–991.
29. Trovatelli, S., Tre fructose-6-phosphate Shunt as peculiar pattern of hexose degradation in the genus Bifidobacterium. Ann. Micr. 15 (1965), 19–29.
30. Lugli, G.A., et al. Comparative genomic and phylogenomic analyses of the Bifidobacteriaceae family. BMC Genomics, 18, 2017, 568.
31. Bottacini, F., et al. Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut. PLoS One, 7, 2012, e44229.
32. Ventura, M., et al. Genomics as a means to understand bacterial phylogeny and ecological adaptation: the case of bifidobacteria. Antonie Van Leeuwenhoek 91 (2007), 351–372.
33. Ventura, M., et al. Host–microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol. 20 (2012), 467–476.
34. Futuyma, D.J., Moreno, G., The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19 (1988), 207–233.
35. Salyers, A.A., et al. Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl. Environ. Microbiol. 33 (1977), 319–322.
36. Lombard, V., et al. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42:Database issue (2014), D490–D495.
37. Pokusaeva, K., et al. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 6 (2011), 285–306.
38. El Kaoutari, A., et al. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11 (2013), 497–504.
39. Duranti, S., et al. Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ. Microbiol. 17 (2015), 2515–2531.
40. Turroni, F., et al. Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: an example of possible human–microbe co-evolution. Gut Microbes 2 (2011), 183–189.
41. Turroni, F., et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 19514–19519.
42. Marcobal, A., et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10 (2011), 507–514.
43. Lewis, Z.T., et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome, 3, 2015, 13.
44. Wada, J., et al. Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl. Environ. Microbiol. 74 (2008), 3996–4004.
45. Tailford, L.E., et al. Mucin glycan foraging in the human gut microbiome. Front. Genet., 6, 2015, 81.
46. Fujita, K., et al. Identification and molecular cloning of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-alpha-N-acetylgalactosaminidase from Bifidobacterium longum. J. Biol. Chem. 280 (2005), 37415–37422.
47. Ashida, H., et al. Two distinct alpha-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology 19 (2009), 1010–1017.
48. Nishimoto, M., Kitaoka, M., Identification of N-acetylhexosamine 1-kinase in the complete lacto-N-biose I/galacto-N-biose metabolic pathway in Bifidobacterium longum. Appl. Environ. Microbiol. 73 (2007), 6444–6449.
49. Ruas-Madiedo, P., et al. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl. Environ. Microbiol. 74 (2008), 1936–1940.
50. Ruiz, L., et al. Evaluation of the ability of Bifidobacterium longum to metabolize human intestinal mucus. FEMS Microbiol. Lett. 314 (2011), 125–130.
51. van der Maarel, M.J., et al. Properties and applications of starch-converting enzymes of the alpha-amylase family. J. Biotechnol. 94 (2002), 137–155.
52. Ze, X., et al. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J. 6 (2012), 1535–1543.
53. D'Elia, J.N., Salyers, A.A., Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J. Bacteriol. 178 (1996), 7180–7186.
54. Scott, K.P., et al. Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. Proc. Natl. Acad. Sci. U. S. A. 108:Suppl. 1 (2011), 4672–4679.
55. Walker, A.W., et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5 (2011), 220–230.
56. Møller, M.S., et al. Recent insight in α-glucan metabolism in probiotic bacteria. Biologia 69 (2014), 713–721.
57. Duranti, S., et al. Exploration of the genomic diversity and core genome of the Bifidobacterium adolescentis phylogenetic group by means of a polyphasic approach. Appl. Environ. Microbiol. 79 (2013), 336–346.
58. Ryan, S.M., et al. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl. Environ. Microbiol. 72 (2006), 5289–5296.
59. Mirande, C., et al. Dietary fibre degradation and fermentation by two xylanolytic bacteria Bacteroides xylanisolvens XB1A and Roseburia intestinalis XB6B4 from the human intestine. J. Appl. Microbiol. 109 (2010), 451–460.
60. Ejby, M., et al. Structural basis for arabinoxylo-oligosaccharide capture by the probiotic Bifidobacterium animalis subsp. lactis Bl-04. Mol. Microbiol. 90 (2013), 1100–1112.
61. Rogowski, A., et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun., 6, 2015, 7481.
62. O'Connell Motherway, M., et al. Metabolism of a plant derived galactose-containing polysaccharide by Bifidobacterium breve UCC2003. Microb. Biotechnol. 4 (2011), 403–416.
63. Pokusaeva, K., et al. Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb. Biotechnol. 3 (2010), 311–323.
64. Pokusaeva, K., et al. Characterization of two novel alpha-glucosidases from Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 75 (2009), 1135–1143.
65. Bottacini, F., et al. Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics, 15, 2014, 170.
66. Egan, M., et al. Glycosulfatase-encoding gene cluster in Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 82 (2016), 6611–6623.
67. Ruiz-Moyano, S., et al. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl. Environ. Microbiol. 79 (2013), 6040–6049.
68. Matsuki, T., et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat. Commun., 7, 2016, 11939.
69. Bunesova, V., et al. Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense. BMC Microbiol., 16, 2016, 248.
70. Maldonado-Gomez, M.X., et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe 20 (2016), 515–526.
71. Ferrario, C., et al. How to feed the mammalian gut microbiota: bacterial and metabolic modulation by dietary fibers. Front Microbiol, 2017, 10.3389/fmicb.2017.01749 Published online September 12, 2017.
72. Pande, S., et al. Metabolic cross-feeding via intercellular nanotubes among bacteria. Nat. Commun., 6, 2015, 6238.
73. Phelan, V.V., et al. Microbial metabolic exchange – the chemotype-to-phenotype link. Nat. Chem. Biol. 8 (2012), 26–35.
74. De Vuyst, L., Leroy, F., Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifdobacterial competitiveness, butyrate production, and gas production. Int. J. Food Microbiol. 149 (2011), 73–80.
75. Barcenilla, A., et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66 (2000), 1654–1661.
76. Morrison, D.J., et al. Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate?. Br. J. Nutr. 96 (2006), 570–577.
77. Duncan, S.H., Flint, H.J., Proposal of a neotype strain (A1-86) for Eubacterium rectale. Request for an opinion. Int. J. Syst. Evol. Microbiol. 58 (2008), 1735–1736.
78. Falony, G., et al. Coculture fermentations of Bifidobacterium species and Bacteroides thetaiotaomicron reveal a mechanistic insight into the prebiotic effect of inulin-type fructans. Appl. Environ. Microbiol. 75 (2009), 2312–2319.
79. Moens, F., et al. Lactate- and acetate-based cross-feeding interactions between selected strains of lactobacilli, bifidobacteria and colon bacteria in the presence of inulin-type fructans. Int. J. Food Microbiol. 241 (2017), 225–236.
80. Garrido, D., et al. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci. Rep., 5, 2015, 13517.
81. Bunesova, V., et al. Mucin cross-feeding of infant bifidobacteria and Eubacterium hallii. Microb. Ecol., 2017, 10.1007/s00248-017-1037-4 Published online July 18, 2017.
82. Schwab, C., et al. Trophic interactions of infant bifidobacteria and Eubacterium hallii during L-fucose and fucosyllactose degradation. Front. Microbiol., 8, 2017, 95.
83. Belenguer, A., et al. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 72 (2006), 3593–3599.
84. Ejby, M., et al. An ATP binding cassette transporter mediates the uptake of alpha-(1,6)-linked dietary oligosaccharides in Bifidobacterium and correlates with competitive growth on these substrates. J. Biol. Chem. 291 (2016), 20220–20231.