دورية أكاديمية

Milk oligosaccharide-driven persistence of Bifidobacterium pseudocatenulatum modulates local and systemic microbial metabolites upon synbiotic treatment in conventionally colonized mice.

التفاصيل البيبلوغرافية
العنوان: Milk oligosaccharide-driven persistence of Bifidobacterium pseudocatenulatum modulates local and systemic microbial metabolites upon synbiotic treatment in conventionally colonized mice.
المؤلفون: Larke JA; Department of Nutrition, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA., Heiss BE; Department of Food Science and Technology, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA., Ehrlich AM; Department of Anatomy, Physiology, and Cell Biology, School of Veterinary Medicine, University of California, Davis, , Davis, CA, USA., Taft DH; Department of Food Science and Technology, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA., Raybould HE; Department of Anatomy, Physiology, and Cell Biology, School of Veterinary Medicine, University of California, Davis, , Davis, CA, USA., Mills DA; Department of Food Science and Technology, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA. damills@ucdavis.edu., Slupsky CM; Department of Nutrition, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA. cslupsky@ucdavis.edu.; Department of Food Science and Technology, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA. cslupsky@ucdavis.edu.
المصدر: Microbiome [Microbiome] 2023 Aug 28; Vol. 11 (1), pp. 194. Date of Electronic Publication: 2023 Aug 28.
نوع المنشور: Video-Audio Media; Journal Article; Research Support, Non-U.S. Gov't; Research Support, N.I.H., Extramural; Research Support, U.S. Gov't, Non-P.H.S.
اللغة: English
بيانات الدورية: Publisher: BioMed Central Country of Publication: England NLM ID: 101615147 Publication Model: Electronic Cited Medium: Internet ISSN: 2049-2618 (Electronic) Linking ISSN: 20492618 NLM ISO Abbreviation: Microbiome Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London: BioMed Central, 2013-
مواضيع طبية MeSH: Bifidobacterium pseudocatenulatum* , Synbiotics* , Actinobacteria*, Humans ; Animals ; Mice ; RNA, Ribosomal, 16S/genetics ; Milk, Human ; Oligosaccharides ; Bifidobacterium ; Prebiotics
مستخلص: Background: Bifidobacteria represent an important gut commensal in humans, particularly during initial microbiome assembly in the first year of life. Enrichment of Bifidobacterium is mediated though the utilization of human milk oligosaccharides (HMOs), as several human-adapted species have dedicated genomic loci for transport and metabolism of these glycans. This results in the release of fermentation products into the gut lumen which may offer physiological benefits to the host. Synbiotic pairing of probiotic species with a cognate prebiotic delivers a competitive advantage, as the prebiotic provides a nutrient niche.
Methods: To determine the fitness advantage and metabolic characteristics of an HMO-catabolizing Bifidobacterium strain in the presence or absence of 2'-fucosyllactose (2'-FL), conventionally colonized mice were gavaged with either Bifidobacterium pseudocatenulatum MP80 (B.p. MP80) (as the probiotic) or saline during the first 3 days of the experiment and received water or water containing 2'-FL (as the prebiotic) throughout the study.
Results: 16S rRNA gene sequencing revealed that mice provided only B.p. MP80 were observed to have a similar microbiota composition as control mice throughout the experiment with a consistently low proportion of Bifidobacteriaceae present. Using 1 H NMR spectroscopy, similar metabolic profiles of gut luminal contents and serum were observed between the control and B.p. MP80 group. Conversely, synbiotic supplemented mice exhibited dramatic shifts in their community structure across time with an overall increased, yet variable, proportion of Bifidobacteriaceae following oral inoculation. Parsing the synbiotic group into high and moderate bifidobacterial persistence based on the median proportion of Bifidobacteriaceae, significant differences in gut microbial diversity and metabolite profiles were observed. Notably, metabolites associated with the fermentation of 2'-FL by bifidobacteria were significantly greater in mice with a high proportion of Bifidobacteriaceae in the gut suggesting metabolite production scales with population density. Moreover, 1,2-propanediol, a fucose fermentation product, was only observed in the liver and brain of mice harboring high proportions of Bifidobacteriaceae.
Conclusions: This study reinforces that the colonization of the gut with a commensal microorganism does not guarantee a specific functional output. Video Abstract.
(© 2023. BioMed Central Ltd., part of Springer Nature.)
References: György P, Norris RF, Rose CS. Bifidus factor. I. A variant of Lactobacillus bifidus requiring a special growth factor. Arch Biochem Biophys. 1954;48:193–201. (PMID: 13125589)
Davis JCC, et al. Identification of Oligosaccharides in feces of breast-fed infants and their correlation with the gut microbial community. Mol Cell Proteomics. 2016;15:2987–3002. (PMID: 274355855013312)
Totten SM, et al. Comprehensive profiles of human milk oligosaccharides yield highly sensitive and specific markers for determining secretor status in lactating mothers. J Proteome Res. 2012;11:6124–33. (PMID: 23140396)
Sakanaka M, et al. Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. Sci Adv. 2019;5:eaaw7696. (PMID: 314893706713505)
Lawson MAE, et al. Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. ISME J. 2020;14:635–48. (PMID: 31740752)
Vatanen T, et al. Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life. Nat Microbiol. 2019;4:470–9. (PMID: 30559407)
Karav S, Casaburi G, Frese SA. Reduced colonic mucin degradation in breastfed infants colonized by Bifidobacterium longum subsp. infantis EVC001. FEBS Open Bio. 2018;8:1649–57. (PMID: 303382166168692)
Casaburi G, et al. Early-life gut microbiome modulation reduces the abundance of antibiotic-resistant bacteria. Antimicrob Resist Infect Control. 2019;8:131. (PMID: 314232986693174)
Matsuki T, et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun. 2016;7:11939. (PMID: 273400924931012)
Henrick BM, et al. Colonization by B. infantis EVC001 modulates enteric inflammation in exclusively breastfed infants. Pediatr Res. 2019;86:749–57. (PMID: 314431026887859)
Lewis ZT, et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome. 2015;3:13. (PMID: 259226654412032)
Vatanen T, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016;165:842–53. (PMID: 271331674950857)
Kalliomäki M, Carmen Collado M, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008;87:534–8. (PMID: 18326589)
Stanislawski MA, et al. Gut microbiota in the first 2 years of life and the association with body mass index at age 12 in a Norwegian birth cohort. mBio. 2018;9:e01751–18.
Huda MN, et al. Bifidobacterium abundance in early infancy and vaccine response at 2 years of age. Pediatrics. 2019;143: e20181489. (PMID: 30674610)
Taft DH, et al. Bifidobacterial dominance of the gut in early life and acquisition of antimicrobial resistance. mSphere. 2018;3:e00441–18.
Nguyen M, et al. Impact of probiotic B. infantis EVC001 feeding in premature infants on the gut microbiome, nosocomially acquired antibiotic resistance, and enteric inflammation. Front Pediatr. 2021;9:618009. (PMID: 336651757921802)
Zmora N, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell. 2018;174:1388–1405.e21. (PMID: 30193112)
Maldonado-Gómez MX, et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe. 2016;20:515–26. (PMID: 27693307)
Martínez I. et al. Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly. eLife. 2018;7:e36521.
Benson AK, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci. 2010;107:18933–8. (PMID: 209378752973891)
Carmody RN, et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe. 2015;17:72–84. (PMID: 25532804)
Suez J, Zmora N, Segal E, Elinav E. The pros, cons, and many unknowns of probiotics. Nat Med. 2019;25:716–29. (PMID: 31061539)
Swanson KS, et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol. 2020;17:687–701. (PMID: 328269667581511)
Bertuzzo E, et al. Spatial effects on species persistence and implications for biodiversity. Proc Natl Acad Sci. 2011;108:4346–51. (PMID: 213681813060266)
Walter J, Maldonado-Gómez MX, Martínez I. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes. Curr Opin Biotechnol. 2018;49:129–39. (PMID: 28866242)
Zhang C, et al. Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME J. 2016;10:2235–45. (PMID: 269535994989305)
Heiss BE, et al. Bifidobacterium catabolism of human milk oligosaccharides overrides endogenous competitive exclusion driving colonization and protection. Gut Microbes. 2021;13:1986666. (PMID: 347056118555557)
Shani G, et al. Fucosylated human milk oligosaccharide foraging within the species Bifidobacterium pseudocatenulatum is driven by glycosyl hydrolase content and specificity. Appl Environ Microbiol. 2022;88:e01707–e1721. (PMID: 347578228788745)
Frese SA, et al. Persistence of supplemented Bifidobacterium longum subsp. infantis EVC001 in breastfed infants. mSphere. 2017;2:e00501–17.
O’Brien CE, et al. Early probiotic supplementation with B. infantis in breastfed infants leads to persistent colonization at 1 year. Pediatr Res. 2021;91:627–636.
Caporaso JG, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci. 2011;108:4516–22. (PMID: 20534432)
Bolyen E, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7. (PMID: 313412887015180)
Callahan BJ, et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. (PMID: 272140474927377)
Quast C, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–6. (PMID: 231932833531112)
R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2020.
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Soft. 2015;67:1–48.
Pustejovsky J. clubSandwich: cluster-robust (Sandwich) variance estimators with small-sample corrections. R package. 2021.
Oksanen J, et al. vegan: community ecology package. R package version 2.5–7. R package version 2.5–7. 2020.
Hervé M. RVAideMemoire: testing and plotting procedures for biostatistics. R package version 0.9–79. 2021.
Morton JT, et al. Establishing microbial composition measurement standards with reference frames. Nat Commun. 2019;10:2719. (PMID: 312220236586903)
Therneau TM, & Atkinson EJ. RPART: recursive partitioning and regression trees. R package version 4.1–15. 2019. https://CRAN.R-project.org/package=rpart .
Davis LMG, Martínez 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. (PMID: 219664543180383)
Mallon CA, van Elsas JD, Salles JF. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol. 2015;23:719–29. (PMID: 26439296)
van Elsas JD, et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci. 2012;109:1159–64. (PMID: 222326693268289)
Chow J, et al. Fecal metabolomics of healthy breast-fed versus formula-fed infants before and during in vitro batch culture fermentation. J Proteome Res. 2014;13:2534–42. (PMID: 24628373)
He X, et al. Fecal microbiome and metabolome of infants fed bovine MFGM supplemented formula or standard formula with breast-fed infants as reference: a randomized controlled trial. Sci Rep. 2019;9:11589. (PMID: 314062306690946)
Flint HJ, Duncan SH, Scott KP, Louis P. Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc. 2015;74:13–22. (PMID: 25268552)
So D, et al. Dietary fiber intervention on gut microbiota composition in healthy adults: a systematic review and meta-analysis. Am J Clin Nutr. 2018;107:965–83. (PMID: 29757343)
Krumbeck JA, Walter J, Hutkins RW. Synbiotics for improved human health: recent developments, challenges, and opportunities. Ann Rev Food Sci Technol. 2018;9:451–79.
Krumbeck JA, Maldonado-Gomez MX, Ramer-Tait AE, Hutkins RW. Prebiotics and synbiotics: dietary strategies for improving gut health. Curr Opin Gastroenterol. 2016;32:110–9. (PMID: 26825589)
Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett. 2009;294:1–8. (PMID: 19222573)
Lee S, et al. 2′-Fucosyllactose supplementation improves gut-brain signaling and diet-induced obese phenotype and changes the gut microbiota in high fat-fed mice. Nutrients. 2020;12:1003. (PMID: 322605637231103)
Marcobal A, Sonnenburg JL. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect. 2012;18:12–5. (PMID: 226470413671919)
Salonen A, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014;8:2218–30. (PMID: 247633704992075)
Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol. 2017;19:29–41. (PMID: 27928878)
Rotimi VO, Duerden BI. Bacteroides species in the normal neonatal faecal flora. J Hyg. 1981;87:299–304. (PMID: 72881812134041)
Marcobal A, et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe. 2011;10:507–14. (PMID: 3227561)
He X, et al. Metabolic phenotype of breast-fed infants, and infants fed standard formula or bovine MFGM supplemented formula: a randomized controlled trial. Sci Rep. 2019;9:339.
Lee H, et al. Milk fat globule membrane as a modulator of infant metabolism and gut microbiota: a formula supplement narrowing the metabolic differences between breastfed and formula-fed infants. Mol Nutr Food Res. 2021;65:2000603.
Larke J, et al. Premature infant fecal metabolite profiles are modulated in a probiotic specific manner. J Pediatr Gastroenterol Nutr. 2022;75:535–42. (PMID: 35881967)
Crovesy L, El-Bacha T, Rosado EL. Modulation of the gut microbiota by probiotics and synbiotics is associated with changes in serum metabolite profile related to a decrease in inflammation and overall benefits to metabolic health: a double-blind randomized controlled clinical trial in women with obesity. Food Funct. 2021;12:2161–70. (PMID: 33565558)
Kuntz S, et al. Metabolic fate and distribution of 2´-fucosyllactose: direct influence on gut microbial activity but not on brain. Mol Nutr Food Res. 2019;63:1900035. (PMID: 311251766618057)
معلومات مُعتمدة: R01 AT008759 United States AT NCCIH NIH HHS; F32HD093185 United States NH NIH HHS; 5T32AI060555 United States NH NIH HHS
فهرسة مساهمة: Keywords: 2′-FL; Colonization; HMO; Human milk oligosaccharide; Mice; Prebiotic; Probiotic
المشرفين على المادة: 0 (RNA, Ribosomal, 16S)
0 (Oligosaccharides)
0 (Prebiotics)
تواريخ الأحداث: Date Created: 20230827 Date Completed: 20230829 Latest Revision: 20231122
رمز التحديث: 20240829
مُعرف محوري في PubMed: PMC10463478
DOI: 10.1186/s40168-023-01624-9
PMID: 37635250
قاعدة البيانات: MEDLINE
الوصف
تدمد:2049-2618
DOI:10.1186/s40168-023-01624-9