Transcriptional analysis of oligosaccharide utilization by Bifidobacterium lactis Bl-04

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Andersen, Joakim M ^a,b   Barrangou, Rodolphe ^c   Hachem, Maher Abou ^a   Lahtinen, Sampo J ^c   Goh, Yong Jun ^b   Svensson, Birte ^a   Klaenhammer, Todd R ^b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c DUPONT COMPANY   (United States)

Author keywords

ABC transporter; Bifidobacterium lactis; Glycoside hydrolase; GPH transporter; Prebiotics; Transcriptomics

Indexed keywords

ABC TRANSPORTER; ALPHA HEXOSE; BETA GALACTOSE OLIGOSACCHARIDE; BETA HEXOSE; BETA XYLO OLIGOSACCHARIDE; BETA XYLOSIDE; BINDING PROTEIN; CELLOBIOSE; GALACTOSIDE; GENTIOBIOSE; GLUCOSIDE; GLYCOSIDASE; GLYCOSIDE; HEXOSE; ISOMALTOSE; MALTOTRIOSE; MELIBIOSE; OLIGOSACCHARIDE; PANOSE; RAFFINOSE; SOLUTE BINDING PROTEIN; STACHYOSE; UNCLASSIFIED DRUG; XYLOBIOSE;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIFIDOBACTERIUM ANIMALIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CATABOLISM; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC ANALYSIS; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN FAMILY; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

BIFIDOBACTERIUM; CELL MEMBRANE; DATA MINING; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENOMICS; MULTIGENE FAMILY; OLIGOSACCHARIDES; PREBIOTICS; TRANSCRIPTION, GENETIC; UP-REGULATION;

BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS;

EID: 84877285435     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-312     Document Type: Article

References (76)

1. Reid G, et al. New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol 2003, 37:105-118. 10.1097/00004836-200308000-00004, 12869879.
2. Turroni F, van Sinderen D, Ventura M. Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 2011, 149:37-44. 10.1016/j.ijfoodmicro.2010.12.010, 21276626.
3. Szajewska H, Guandalini S, Morelli L, Van Goudoever JB, Walker A. Effect of Bifidobacterium animalis subsp. lactis supplementation in preterm infants: A systematic review of randomized controlled trials. J Pediatr Gastroenterol Nutr 2010, 51:203-209. 10.1097/MPG.0b013e3181dc0d93, 20543719.
4. Waller PA, et al. Dose-response effect of Bifidobacterium lactis HN019 on whole gut transit time and functional gastrointestinal symptoms in adults. Scand J Gastroenterol 2011, 46:1057-1064. 10.3109/00365521.2011.584895, 3171707, 21663486.
5. Ganguli K, Walker WA. Probiotics in the prevention of necrotizing enterocolitis. J Clin Gastroenterol 2011, 45(Suppl):S133-138.
6. Steed H, et al. Clinical trial: The microbiological and immunological effects of synbiotic consumption - a randomized double-blind placebo-controlled study in active crohn's disease. Aliment Pharmacol Ther 2010, 32:872-883. 10.1111/j.1365-2036.2010.04417.x, 20735782.
7. Ouwehand AC, et al. Bifidobacterium microbiota and parameters of immune function in elderly subjects. FEMS Immunol Med Microbiol 2008, 53:18-25. 10.1111/j.1574-695X.2008.00392.x, 18336547.
8. Ventura M, et al. Genome-scale analyses of health-promoting bacteria: Probiogenomics. Nat Rev Microbiol 2009, 7:61-71. 10.1038/nrmicro2047, 19029955.
9. Bottacini F, et al. Comparative genomics of the genus Bifidobacterium. Microbiology 2010, 156:3243-3254. 10.1099/mic.0.039545-0, 20634238.
10. Turroni F, et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA 2010, 107:19514-19519. 10.1073/pnas.1011100107, 2984195, 20974960.
11. Schell M, et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci USA 2002, 99:14422-14427. 10.1073/pnas.212527599, 137899, 12381787.
12. González R, Klaassens ES, Malinen E, de Vos W,M. & Vaughan EE Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide. Appl Environ Microbiol 2008, 74:4686-4694. 10.1128/AEM.00122-08, 2519361, 18539808, de Vos W,M. & Vaughan EE.
13. Turroni F, et al. Diversity of bifidobacteria within the infant gut microbiota. PLoS One 2012, 7:e36957. 10.1371/journal.pone.0036957, 3350489, 22606315.
14. Klaassens ES, et al. Mixed-species genomic microarray analysis of fecal samples reveals differential transcriptional responses of bifidobacteria in breast- and formula-fed infants. Appl Environ Microbiol 2009, 75:2668-2676. 10.1128/AEM.02492-08, 2681671, 19286790.
15. Davis LM, Martinez I, Walter J, Goin C, Hutkins RW. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One 2011, 6:e25200. 10.1371/journal.pone.0025200, 3180383, 21966454.
16. Roberfroid M. Prebiotics: The concept revisited. J Nutr 2007, 137:830S-837S.
17. Roberfroid M, et al. Prebiotic effects: Metabolic and health benefits. Br J Nutr 2010, 104(Suppl 2):S1-S63.
18. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid M. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics. Nutr Res Rev 2004, 17:259-275. 10.1079/NRR200479, 19079930.
19. Makelainen H, Hasselwander O, Rautonen N, Ouwehand AC. Panose, a new prebiotic candidate. Lett Appl Microbiol 2009, 49:666-672. 10.1111/j.1472-765X.2009.02698.x, 19874483.
20. van den Broek LA, Hinz SW, Beldman G, Vincken JP, Voragen AG. Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res 2008, 52:146-163. 10.1002/mnfr.200700121, 18040988.
21. Pokusaeva K, Fitzgerald GF, van Sinderen D. Carbohydrate metabolism in bifidobacteria. Genes & Nutrition 2011, 6:285-306. 10.1007/s12263-010-0206-6, 3678022, 23766960.
22. Paineau D, et al. Effects of seven potential probiotic strains on specific immune responses in healthy adults: A double-blind, randomized, controlled trial. FEMS Immunol Med Microbiol 2008, 53:107-113. 10.1111/j.1574-695X.2008.00413.x, 18422632.
23. Ouwehand AC, et al. Specific probiotics alleviate allergic rhinitis during the birch pollen season. World J Gastroenterol 2009, 15:3261-3268. 10.3748/wjg.15.3261, 2710782, 19598302.
24. Bartosch S, Woodmansey EJ, Paterson JC, McMurdo ME, Macfarlane GT. Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis, and oligofructose in elderly persons, determined by real-time polymerase chain reaction and counting of viable bacteria. Clin Infect Dis 2005, 40:28-37. 10.1086/426027, 15614689.
25. Barrangou R, et al. Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J Bacteriol 2009, 191:4144-4151. 10.1128/JB.00155-09, 2698493, 19376856.
26. van Zanten GC, et al. The effect of selected synbiotics on microbial composition and short-chain fatty acid production in a model system of the human colon. PLoS One 2012, 7(10):e47212. 10.1371/journal.pone.0047212, 3474826, 23082149.
27. Tatusov RL, et al. The COG database: An updated version includes eukaryotes. BMC Bioinforma 2003, 4:41.
28. Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science 2010, 327:167-170. 10.1126/science.1179555, 20056882.
29. Gilad O, et al. Insights into physiological traits of Bifidobacterium animalis subsp. lactis BB-12 through membrane proteome analysis. J Proteomics 2012, 75:1190-200. 10.1016/j.jprot.2011.10.031, 22119884.
30. Cantarel BL, et al. The carbohydrate-active EnZymes database (CAZy): An expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-238. 10.1093/nar/gkn663, 2686590, 18838391.
31. Saier MH, Yen MR, Noto K, Tamang DG, Elkan C. The transporter classification database: Recent advances. Nucleic Acids Res 2009, 37:D274-278. 10.1093/nar/gkn862, 2686586, 19022853.
32. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786. 10.1038/nmeth.1701, 21959131.
33. St John FJ, Gonzalez JM, Pozharski E. Consolidation of glycosyl hydrolase family 30: A dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett 2010, 584:4435-4441. 10.1016/j.febslet.2010.09.051, 20932833.
34. Shipkowski S, Brenchley JE. Bioinformatic, genetic, and biochemical evidence that some glycoside hydrolase family 42 beta-galactosidases are arabinogalactan type I oligomer hydrolases. Appl Environ Microbiol 2006, 72:7730-7738. 10.1128/AEM.01306-06, 1694227, 17056685.
35. Parche S, et al. Sugar transport systems of Bifidobacterium longum NCC2705. J Mol Microbiol Biotechnol 2007, 12:9-19. 10.1159/000096455, 17183207.
36. O'Connell Motherway M, Kinsella M, Fitzgerald GF, van Sinderen D. Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb Biotechnol 2013, 6(1):67-79. 10.1111/1751-7915.12011, 23199239.
37. Lagaert S, et al. Substrate specificity of three recombinant α-l-arabinofuranosidases from Bifidobacterium adolescentis and their divergent action on arabinoxylan and arabinoxylan oligosaccharides. Biochem Biophys Res Commun 2010, 402:644-650. 10.1016/j.bbrc.2010.10.075, 20971079.
38. Lagaert S, et al. Recombinant expression and characterization of a reducing-end xylose-releasing exo-oligoxylanase from Bifidobacterium adolescentis. Appl Environ Microbiol 2007, 73:5374-5377. 10.1128/AEM.00722-07, 1950967, 17586675.
39. Liu D, et al. Proteomics analysis of Bifidobacterium longum NCC2705 growing on glucose, fructose, mannose, xylose, ribose, and galactose. Proteomics 2011, 11:2628-2638. 10.1002/pmic.201100035, 21630463.
40. Taylor EJ, et al. Structure and activity of two metal ion-dependent acetylxylan esterases involved in plant cell wall degradation reveals a close similarity to peptidoglycan deacetylases. J Biol Chem 2006, 281:10968-10975. 10.1074/jbc.M513066200, 16431911.
41. Nakai H, et al. The maltodextrin transport system and metabolism in Lactobacillus acidophilus NCFM and production of novel alpha-glucosides through reverse phosphorolysis by maltose phosphorylase. FEBS J 2009, 276:7353-7365. 10.1111/j.1742-4658.2009.07445.x, 19919544.
42. Monedero V, Yebra MJ, Poncet S, Deutscher J. Maltose transport in Lactobacillus casei and its regulation by inducer exclusion. Res Microbiol 2008, 159:94-102. 10.1016/j.resmic.2007.10.002, 18096372.
43. Ajdic D, Pham VT. Global transcriptional analysis of Streptococcus mutans sugar transporters using microarrays. J Bacteriol 2007, 189:5049-5059. 10.1128/JB.00338-07, 1951856, 17496079.
44. Fredslund F, et al. Crystal structure of alpha-galactosidase from Lactobacillus acidophilus NCFM: Insight into tetramer formation and substrate binding. J Mol Biol 2011, 412:466-480. 10.1016/j.jmb.2011.07.057, 21827767.
45. Pokusaeva K, O'Connell-Motherway M, Zomer A, Fitzgerald GF, van Sinderen D. Characterization of two novel alpha-glucosidases from Bifidobacterium breve UCC2003. Appl Environ Microbiol 2009, 75:1135-1143. 10.1128/AEM.02391-08, 2643558, 19114534.
46. Meile L, Rohr LM, Geissmann TA, Herensperger M, Teuber M. Characterization of the D-xylulose 5-phosphate/D-fructose 6-phosphate phosphoketolase gene (xfp) from Bifidobacterium lactis. J Bacteriol 2001, 183:2929-2936. 10.1128/JB.183.9.2929-2936.2001, 99511, 11292814.
47. Law CJ, Maloney PC, Wang DN. Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 2008, 62:289-305. 10.1146/annurev.micro.61.080706.093329, 2612782, 18537473.
48. Oldham ML, Khare D, Fa Q, Davidson AL, Chen J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 2007, 450:515-521. 10.1038/nature06264, 18033289.
49. Espinosa M, Puyet A. The maltose / maltodextrin regulon of Streptococcus pneumoniae. Biochemistry (N Y ) 1997, 272:30860-30865.
50. Berntsson RP, Smits SHJ, Schmitt L, Slotboom D, Poolman B. A structural classification of substrate-binding proteins. FEBS Lett 2010, 584:2606-2617. 10.1016/j.febslet.2010.04.043, 20412802.
51. Cani PD, Delzenne NM. The gut microbiome as therapeutic target. Pharmacol Ther 2011, 130:202-212. 10.1016/j.pharmthera.2011.01.012, 21295072.
52. Macfarlane GT, Steed H, Macfarlane S. Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J Appl Microbiol 2008, 104:305-344.
53. Turroni F, et al. Analysis of predicted carbohydrate transport systems encoded by Bifidobacterium bifidum PRL2010. Appl Environ Microbiol 2012, 78:5002-5012. 10.1128/AEM.00629-12, 3416360, 22562993.
54. Audy J, Labrie S, Roy D, Lapointe G. Sugar source modulates exopolysaccharide biosynthesis in Bifidobacterium longum subsp. longum CRC 002. Microbiology 2010, 156:653-664. 10.1099/mic.0.033720-0, 19850611.
55. Fukuda S, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011, 469:543-547. 10.1038/nature09646, 21270894.
56. Marion C, Aten AE, Sa W, King SJ. Identification of an ATPase, MsmK, which energizes multiple carbohydrate ABC transporters in Streptococcus pneumoniae. Infect Immun 2011, 79:4193-4200. 10.1128/IAI.05290-11, 3187249, 21825065.
57. Barrangou R, et al. Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc Natl Acad Sci USA 2006, 103:3816-3821. 10.1073/pnas.0511287103, 1533782, 16505367.
58. Martens EC, et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 2011, 9:e1001221. 10.1371/journal.pbio.1001221, 3243724, 22205877.
59. Pokusaeva K, Connell-motherway M, Zomer A, Fitzgerald GF, Sinderen DV. Cellodextrin utilization by Bifidobacterium breve UCC2003. Appl Environ Microbiol 2011, 77:1681-1690. 10.1128/AEM.01786-10, 3067287, 21216899.
60. Gilad O, et al. Combined transcriptome and proteome analysis of Bifidobacterium animalis subsp. lactis BB-12 grown on xylo-oligosaccharides and a model of their utilization. Appl Environ Microbiol 2010, 76:7285-7291. 10.1128/AEM.00738-10, 2976271, 20851982.
61. Kabel M, et al. Biochemical characterization and relative expression levels of multiple carbohydrate esterases of the xylanolytic rumen bacterium Prevotella ruminicola 23 grown on an ester-enriched substrate. Appl Environ Microbiol 2011, 77:5671-5681. 10.1128/AEM.05321-11, 3165261, 21742923.
62. Fushinobu S. Unique sugar metabolic pathways of bifidobacteria. Biosci Biotechnol Biochem 2010, 74:2374-2384. 10.1271/bbb.100494, 21150123.
63. Barrangou R, Altermann E, Hutkins R, Cano R, Klaenhammer TR. Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc Natl Acad Sci USA 2003, 100:8957-8962. 10.1073/pnas.1332765100, 166420, 12847288.
64. Daniels L, Zeikus JG. Improved culture flask for obligate anaerobes. Appl Microbiol 1975, 29:710-711. 187062, 807163.
65. Goh YJ, et al. Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 2009, 75:3093-3105. 10.1128/AEM.02502-08, 2681627, 19304841.
66. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
67. Larkin MA, et al. Clustal W and clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404, 17846036.
68. Huson DH, et al. Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinforma 2007, 8:460.
69. Wei X, et al. Fructose uptake in Bifidobacterium longum NCC2705 is mediated by an ATP-binding cassette transporter. J Biol Chem 2012, 287:357-367. 10.1074/jbc.M111.266213, 3249088, 22102285.
70. Andersen JM, et al. Transcriptional and functional analysis of galactooligosaccharide uptake by lacS in Lactobacillus acidophilus. Proc Natl Acad Sci USA 2011, 108:17785-17790. 10.1073/pnas.1114152108, 3203779, 22006318.
71. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction-the phobius web server. Nucleic Acids Res 2007, 35:W429-32. 10.1093/nar/gkm256, 1933244, 17483518.
72. Gopal S, et al. Maltose and maltodextrin utilization by Listeria monocytogenes depend on an inducible ABC transporter which is repressed by glucose. PLoS One 2010, 5:e10349. 10.1371/journal.pone.0010349, 2860498, 20436965.
73. Abbott DW, et al. The molecular basis of glycogen breakdown and transport in Streptococcus pneumoniae. Mol Microbiol 2010, 77:183-199. 10.1111/j.1365-2958.2010.07199.x, 2911477, 20497336.
74. Schanert S, et al. Maltose and maltodextrin utilization by Bacillus subtilis. J Bacteriol 2006, 188:3911-3922. 10.1128/JB.00213-06, 1482931, 16707683.
75. Garrido D, Kim JH, German JB, Raybould HE, Mills DA. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One 2011, 6:e17315. 10.1371/journal.pone.0017315, 3057974, 21423604.
76. Suzuki R, et al. Structural and thermodynamic analyses of solute-binding protein from Bifidobacterium longum specific for core 1 disaccharide and lacto-N-biose I. J Biol Chem 2008, 283:13165-13173. 10.1074/jbc.M709777200, 18332142.