Bifidobacterium response to lactulose ingestion in the gut relies on a solute-binding protein-dependent ABC transporter.
ATP-Binding Cassette Transporters
/ metabolism
Adolescent
Adult
Aged
Aged, 80 and over
Bacterial Proteins
/ metabolism
Bifidobacterium
/ drug effects
Cross-Sectional Studies
Feces
/ microbiology
Female
Gastrointestinal Agents
/ administration & dosage
Gastrointestinal Microbiome
/ drug effects
Gastrointestinal Tract
/ drug effects
Humans
Lactulose
/ administration & dosage
Middle Aged
Young Adult
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
10 05 2021
10 05 2021
Historique:
received:
15
06
2020
accepted:
31
03
2021
entrez:
11
5
2021
pubmed:
12
5
2021
medline:
10
8
2021
Statut:
epublish
Résumé
This study aims to understand the mechanistic basis underlying the response of Bifidobacterium to lactulose ingestion in guts of healthy Japanese subjects, with specific focus on a lactulose transporter. An in vitro assay using mutant strains of Bifidobacterium longum subsp. longum 105-A shows that a solute-binding protein with locus tag number BL105A_0502 (termed LT-SBP) is primarily involved in lactulose uptake. By quantifying faecal abundance of LT-SBP orthologues, which is defined by phylogenetic analysis, we find that subjects with 10
Identifiants
pubmed: 33972677
doi: 10.1038/s42003-021-02072-7
pii: 10.1038/s42003-021-02072-7
pmc: PMC8110962
doi:
Substances chimiques
ATP-Binding Cassette Transporters
0
Bacterial Proteins
0
Gastrointestinal Agents
0
Lactulose
4618-18-2
Banques de données
UMIN-CTR
['UMIN000027305']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
541Références
Yachida, S. et al. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat. Med. 25, 968–976 (2019).
pubmed: 31171880
doi: 10.1038/s41591-019-0458-7
Ridaura, V. K. et al. Cultured gut microbiota from twins discordant for obesity modulate adiposity and metabolic phenotypes in mice. Science (80-.) 341, 1–22 (2014).
Stecher, B. et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog. 6, e1000711 (2010).
pubmed: 20062525
pmcid: 2796170
doi: 10.1371/journal.ppat.1000711
Dicksved, J., Ellström, P., Engstrand, L. & Rautelin, H. Susceptibility to campylobacter infection is associated with the species composition of the human fecal microbiota. MBio 5, 1–7 (2014).
doi: 10.1128/mBio.01212-14
Brusaferro, A. et al. Is it time to use probiotics to prevent or treat obesity? Nutrients 10, 1613 (2018).
pmcid: 6266556
doi: 10.3390/nu10111613
Xiao, J. Z. et al. Probiotics in the treatment of Japanese cedar pollinosis: a double-blind placebo-controlled trial. Clin. Exp. Allergy 36, 1425–1435 (2006).
pubmed: 17083353
doi: 10.1111/j.1365-2222.2006.02575.x
Kobayashi, Y. et al. Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer’s disease. Sci. Rep. 7, 13510 (2017).
pubmed: 29044140
pmcid: 5647431
doi: 10.1038/s41598-017-13368-2
Liu, F. et al. Fructooligosaccharide (FOS) and galactooligosaccharide (GOS) Increase Bifidobacterium but reduce butyrate producing bacteria with adverse glycemic metabolism in healthy young population. Sci. Rep. 7, 1–12 (2017).
Sakai, Y. et al. Prebiotic effect of two grams of lactulose in healthy Japanese women: a randomised, double-blind, placebo-controlled crossover trial. Benef. Microbes 10, 629–639 (2019).
pubmed: 31131617
doi: 10.3920/BM2018.0174
Wesselius-De Casparis, A., Braadbaart, S., Bergh-Bohlken, G. E. & Mimica, M. Treatment of chronic constipation with lactulose syrup: results of a double-blind study. Gut 9, 84–86 (1968).
pubmed: 4867936
pmcid: 1552607
doi: 10.1136/gut.9.1.84
Bouhnik, Y. et al. Lactulose ingestion increases faecal bifidobacterial counts: a randomised double-blind study in healthy humans. Eur. J. Clin. Nutr. 58, 462–466 (2004).
pubmed: 14985684
doi: 10.1038/sj.ejcn.1601829
Bothe, M. et al. Dose-dependent prebiotic effect of lactulose in a computer-controlled in vitro model of the human large intestine. Nutrients 9, 767 (2017).
pmcid: 5537881
doi: 10.3390/nu9070767
Tayebi-Khosroshahi, H. et al. The effect of lactulose supplementation on fecal microflora of patients with chronic kidney disease; a randomized clinical trial. J. Ren. Inj. Prev. 5, 162–167 (2016).
pubmed: 27689115
doi: 10.15171/jrip.2016.34
pmcid: 5040005
Tamura, Y., Mizota, T., Shimamura, S. & Tomita, M. Lactulose and its application to the food and pharmaceutical industries. Bull. Int. Dairy Fed 289, 43–53 (1993).
Matson, V. et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science (80-.) 359, 104–108 (2018).
doi: 10.1126/science.aao3290
Gopalakrishnan, V. et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science (80-.) 359, 97–103 (2018).
doi: 10.1126/science.aan4236
Routy, B. et al. Gut microbiome influences efficacy of PD-1–based immunotherapy against epithelial tumors. Science (80-.) 359, 91–97 (2018).
doi: 10.1126/science.aan3706
Kovatcheva-Datchary, P. et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 22, 971–982 (2015).
pubmed: 26552345
doi: 10.1016/j.cmet.2015.10.001
Sakai, Y. et al. A study of the prebiotic effect of lactulose at low dosages in healthy Japanese women. Biosci. Microbiota Food Health. 38, 69–72 (2019).
pubmed: 31106110
doi: 10.12938/bmfh.18-013
Sotoya, H. et al. Identification of genes involved in galactooligosaccharide utilization in Bifidobacterium breve strain YIT 4014T. Microbiology 163, 1420–1428 (2017).
pubmed: 28920844
doi: 10.1099/mic.0.000517
Shigehisa, A. et al. Characterization of a bifidobacterial system that utilizes galacto-oligosaccharides. Microbiology 161, 1463–1470 (2015).
pubmed: 25903756
pmcid: 4635504
doi: 10.1099/mic.0.000100
Bottacini, F. et al. Comparative genomics and genotype-phenotype associations in Bifidobacterium breve. Sci. Rep. 8, 10633 (2018).
pubmed: 30006593
pmcid: 6045613
doi: 10.1038/s41598-018-28919-4
Ejby, M. et al. An ATP binding cassette transporter mediates the uptake of α-(1,6)-linked dietary oligosaccharides in bifidobacterium and correlates with competitive growth on these substrates. J. Biol. Chem. 291, 20220–20231 (2016).
pubmed: 27502277
pmcid: 5025704
doi: 10.1074/jbc.M116.746529
O’Connell Motherway, M., Kinsella, M., Fitzgerald, G. F. & van Sinderen, D. Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb. Biotechnol. 6, 67–79 (2013).
pubmed: 23199239
doi: 10.1111/1751-7915.12011
Theilmann, M. C., Fredslund, F., Svensson, B., Lo Leggio, L. & Abou Hachem, M. Substrate preference of an ABC importer corresponds to selective growth on β-(1,6)-galactosides in Bifidobacterium animalis subsp. lactis. J. Biol. Chem. 294, 11701–11711 (2019).
pubmed: 31186348
pmcid: 6682729
doi: 10.1074/jbc.RA119.008843
Sakai, Y. et al. Lactulose ingestion causes an increase in the abundance of gut-resident bifidobacteria in Japanese women: a randomised, double-blind, placebo-controlled crossover trial. Benef. Microbes 12, 43–53 (2021).
pubmed: 33393445
doi: 10.3920/BM2020.0100
Nishijima, S. et al. The gut microbiome of healthy Japanese and its microbial and functional uniqueness. DNA Res. 23, 125–133 (2016).
pubmed: 26951067
pmcid: 4833420
doi: 10.1093/dnares/dsw002
Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).
pubmed: 20203603
pmcid: 3779803
doi: 10.1038/nature08821
Ruiz-Aceituno, L., Esteban-Torres, M., James, K., Moreno, F. J. & van Sinderen, D. Metabolism of biosynthetic oligosaccharides by human-derived Bifidobacterium breve UCC2003 and Bifidobacterium longum NCIMB 8809. Int. J. Food Microbiol. 316, 108476 (2020).
pubmed: 31874325
doi: 10.1016/j.ijfoodmicro.2019.108476
Chen, C., Malek, A. A., Wargo, M. J., Hogan, D. A. & Beattie, G. A. The ATP-binding cassette transporter Cbc (choline/betaine/carnitine) recruits multiple substrate-binding proteins with strong specificity for distinct quaternary ammonium compounds. Mol. Microbiol. 75, 29–45 (2010).
pubmed: 19919675
doi: 10.1111/j.1365-2958.2009.06962.x
Odamaki, T. et al. Genomic diversity and distribution of Bifidobacterium longum subsp. longum across the human lifespan. Sci. Rep. 8, 85 (2018).
pubmed: 29311585
pmcid: 5758520
doi: 10.1038/s41598-017-18391-x
Kato, K. et al. Age-related changes in the composition of gut Bifidobacterium species. Curr. Microbiol. 74, 987–995 (2017).
pubmed: 28593350
pmcid: 5486783
doi: 10.1007/s00284-017-1272-4
Gavini, F. et al. Differences in the distribution of bifidobacterial and enterobacterial species in human faecal microflora of three different (children, adults, elderly) age groups. Microb. Ecol. Health Dis. 13, 40–45 (2001).
Polyviou, T. et al. Randomised clinical study: inulin short-chain fatty acid esters for targeted delivery of short-chain fatty acids to the human colon. Aliment. Pharmacol. Ther. 44, 662–672 (2016).
pubmed: 27464984
pmcid: 5026196
doi: 10.1111/apt.13749
Wong, J. M. W., de Souza, R., Kendall, C. W. C., Emam, A. & Jenkins, D. J. A. Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol. 40, 235–243 (2006).
pubmed: 16633129
doi: 10.1097/00004836-200603000-00015
Odamaki, T. et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 16, 90 (2016).
pubmed: 27220822
pmcid: 4879732
doi: 10.1186/s12866-016-0708-5
Sakanaka, M. et al. Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. Sci. Adv. 5, eaaw7696 (2019).
pubmed: 31489370
pmcid: 6713505
doi: 10.1126/sciadv.aaw7696
Matsumura, H., Takeuchi, A. & Kano, Y. Construction of Escherichia coli–Bifidobacterium longum shuttle vector transforming B. longum 105-A and 108-A. Biosci. Biotechnol. Biochem. 61, 1211–1212 (1997).
pubmed: 9255988
doi: 10.1271/bbb.61.1211
Hirayama, Y. et al. Development of a double-crossover markerless gene deletion system in Bifidobacterium longum: functional analysis of the α-galactosidase gene for raffinose assimilation. Appl. Environ. Microbiol. 78, 4984–4994 (2012).
pubmed: 22582061
pmcid: 3416363
doi: 10.1128/AEM.00588-12
Kanesaki, Y. et al. Complete genome sequence of Bifidobacterium longum 105-A, a strain with high transformation efficiency. Genome Announc. 2, 1–2 (2014).
doi: 10.1128/genomeA.01311-14
Sakurama, H. et al. Lacto-N-biosidase encoded by a novel gene of Bifidobacterium longum subspecies longum shows unique substrate specificity and requires a designated chaperone for its active expression. J. Biol. Chem. 288, 25194–25206 (2013).
pubmed: 23843461
pmcid: 3757183
doi: 10.1074/jbc.M113.484733
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10 (2011).
doi: 10.14806/ej.17.1.200
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
R Core Team. R: A language and environment for statistical computing (2020).
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometr J. 50, 346–363 (2008).
doi: 10.1002/bimj.200810425