Impact of short-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 3, 2017, Pages E367-E375

  Azcarate Peril, M Andrea ^a   Ritter, Andrew J ^b   Savaiano, Dennis ^c   Monteagudo Mera, Andrea ^a   Anderson, Carlton ^a   Magness, Scott T ^a   Klaenhammer, Todd R ^d  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Ritter Pharmaceuticals   (United States)

^c PURDUE UNIVERSITY   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

GOS; Lactose intolerance; Microbiome; Prebiotic

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA; CORN SYRUP; GALACTOSE OLIGOSACCHARIDE; LACTOSE; RNA 16S; RP G 28; UNCLASSIFIED DRUG; OLIGOSACCHARIDE; RP-G28;

ACTINOBACTERIA; ADULT; BACTERIUM DETECTION; BIFIDOBACTERIUM; CARBOHYDRATE METABOLISM; CONFERENCE PAPER; CONTROLLED STUDY; DAIRY PRODUCT; DIET THERAPY; DRUG DOSE INCREASE; FAECALIBACTERIUM; FEMALE; FOOD INTAKE; FUSOBACTERIA; HIGH THROUGHPUT SEQUENCING; HUMAN; IN VIVO STUDY; INTESTINE FLORA; LACTOBACILLUS; LACTOSE INTOLERANCE; LACTOSE TOLERANCE; MAJOR CLINICAL STUDY; MALE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; QUANTITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; ROSEBURIA; COLON; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; FECES; METABOLISM; MICROBIOLOGY;

ADULT; BIFIDOBACTERIUM; COLON; DOUBLE-BLIND METHOD; FAECALIBACTERIUM; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; LACTOBACILLUS; LACTOSE; MALE; OLIGOSACCHARIDES; RNA, RIBOSOMAL, 16S;

EID: 85009729394     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1606722113     Document Type: Article

References (48)

1. Itan Y, Jones BL, Ingram CJ, Swallow DM, Thomas MG (2010) A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evol Biol 10:36.
2. Scrimshaw NS, Murray EB (1988) The acceptability of milk and milk products in populations with a high prevalence of lactose intolerance. Am J Clin Nutr 48(4, Suppl): 1079-1159.
3. Hertzler SR, Savaiano DA, Levitt MD (1997) Fecal hydrogen production and consumption measurements. Response to daily lactose ingestion by lactose maldigesters. Dig Dis Sci 42(2):348-353.
4. Savaiano DA, et al. (2013) Improving lactose digestion and symptoms of lactose intolerance with a novel galacto-oligosaccharide (RP-G28): A randomized, double-blind clinical trial. Nutr J 12:160.
5. Davis LM, Martínez I, Walter J, Goin C, Hutkins RW (2011) Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One 6(9):e25200.
6. Andersen JM, et al. (2011) Transcriptional and functional analysis of galactooligosaccharide uptake by lacS in Lactobacillus acidophilus. Proc Natl Acad Sci USA 108(43):17785-17790.
7. Qin J, et al.; MetaHIT Consortium (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59-65.
8. Sim K, et al. (2012) Improved detection of bifidobacteria with optimised 16S rRNAgene based pyrosequencing. PLoS One 7(3):e32543.
9. Sokol H, et al. (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105(43):16731-16736.
10. Hansen R, et al. (2012) Microbiota of de-novo pediatric IBD: Increased Faecalibacterium prausnitzii and reduced bacterial diversity in Crohn's but not in ulcerative colitis. Am J Gastroenterol 107(12):1913-1922.
11. Kostic AD, et al. (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22(2):292-298.
12. Castellarin M, et al. (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22(2):299-306.
13. McCoy AN, et al. (2013) Fusobacterium is associated with colorectal adenomas. PLoS One 8(1):e53653.
14. Langille MG, et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814-821.
15. Tzortzis G, Goulas AK, Baillon ML, Gibson GR, Rastall RA (2004) In vitro evaluation of the fermentation properties of galactooligosaccharides synthesised by alpha-galactosidase from Lactobacillus reuteri. Appl Microbiol Biotechnol 64(1):106-111.
16. Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR (2008) Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr 88(5):1438-1446.
17. Daly K, et al. (2014) Dietary supplementation with lactose or artificial sweetener enhances swine gut Lactobacillus population abundance. Br J Nutr 111(Suppl 1): S30-S35.
18. David LA, et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559-563.
19. Wang F, et al. (2015) Qualitative and semiquantitative analysis of fecal Bifidobacterium species in centenarians living in Bama, Guangxi, China. Curr Microbiol 71(1): 143-149.
20. Klaenhammer TR, Barrangou R, Buck BL, Azcarate-Peril MA, Altermann E (2005) Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol Rev 29(3):393-409.
21. Azcárate-Peril MA, Sikes M, Bruno-Bárcena JM (2011) The intestinal microbiota, gastrointestinal environment and colorectal cancer: A putative role for probiotics in prevention of colorectal cancer? Am J Physiol Gastrointest Liver Physiol 301(3):G401-G424.
22. King S, Glanville J, Sanders ME, Fitzgerald A, Varley D (2014) Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: A systematic review and meta-analysis. Br J Nutr 112(1):41-54.
23. Petrova MI, Lievens E, Malik S, Imholz N, Lebeer S (2015) Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol 6:81.
24. Machiels K, et al. (2014) A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63(8):1275-1283.
25. Lopez-Siles M, et al. (2012) Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and hostderived substrates for growth. Appl Environ Microbiol 78(2):420-428.
26. Goodrich JK, et al. (2014) Human genetics shape the gut microbiome. Cell 159(4): 789-799.
27. Zoetendal EG, Plugge CM, Akkermans AD, de Vos WM (2003) Victivallis vadensis gen. nov., sp. nov., a sugar-fermenting anaerobe from human faeces. Int J Syst Evol Microbiol 53(Pt 1):211-215.
28. Azcarate-Peril MA, et al. (2011) Acute necrotizing enterocolitis of preterm piglets is characterized by dysbiosis of ileal mucosa-associated bacteria. Gut Microbes 2(4): 234-243.
29. Devine AA, et al. (2013) Impact of ileocecal resection and concomitant antibiotics on the microbiome of the murine jejunum and colon. PLoS One 8(8):e73140.
30. Thompson AL, Monteagudo-Mera A, Cadenas MB, Lampl ML, Azcarate-Peril MA (2015) Milk- and solid-feeding practices and daycare attendance are associated with differences in bacterial diversity, predominant communities, and metabolic and immune function of the infant gut microbiome. Front Cell Infect Microbiol 5:3.
31. Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17(19):7843-7853.
32. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105(46): 17994-17999.
33. Caporaso JG, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335-336.
34. Haas BJ, et al.; Human Microbiome Consortium (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21(3):494-504.
35. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460-2461.
36. Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5(3):e9490.
37. Lozupone C, Hamady M, Knight R (2006) UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371.
38. Abubucker S, et al. (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLOS Comput Biol 8(6):e1002358.
39. Monteagudo-Mera A, et al. (2016) High purity galacto-oligosaccharides enhance specific Bifidobacterium species and their metabolic activity in the mouse gut microbiome. Benef Microbes 7(2):247-264.
40. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408.
41. Kent AD, Smith DJ, Benson BJ, Triplett EW (2003) Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl Environ Microbiol 69(11):6768-6776.
42. Johnson MC, Devine AA, Ellis JC, Grunden AM, Fellner V (2009) Effects of antibiotics and oil on microbial profiles and fermentation in mixed cultures of ruminal microorganisms. J Dairy Sci 92(9):4467-4480.
43. Li F, Hullar MA, Lampe JW (2007) Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J Microbiol Methods 68(2): 303-311.
44. Osborne CA, Rees GN, Bernstein Y, Janssen PH (2006) New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl Environ Microbiol 72(2):1270-1278.
45. Junick J, Blaut M (2012) Quantification of human fecal bifidobacterium species by use of quantitative real-time PCR analysis targeting the groEL gene. Appl Environ Microbiol 78(8):2613-2622.
46. Matsuki T, et al. (2004) Quantitative PCR with 16S rRNA-gene-targeted species-specific primers for analysis of human intestinal bifidobacteria. Appl Environ Microbiol 70(1): 167-173.
47. Hermann-Bank ML, Skovgaard K, Stockmarr A, Larsen N, Molbak L (2013) The Gut Microbiotassay: A high-throughput qPCR approach combinable with next generation sequencing to study gut microbial diversity. BMC Genomics 14:788.
48. Kwon H-S, et al. (2006) Rapid identification of potentially probiotic Bifidobacterium species by multiplex PCR using species-specific primers based on the region extending from 16S rRNA through 23 S rRNA. FEMS Microbiol Lett 250(1):55-62.