Most cited article - PubMed ID 28194144
Trophic Interactions of Infant Bifidobacteria and Eubacterium hallii during L-Fucose and Fucosyllactose Degradation
Previous studies indicated an intrinsic relationship between infant diet, intestinal microbiota composition and fermentation activity with a strong focus on the role of breastfeeding on microbiota composition. Yet, microbially formed short-chain fatty acids acetate, propionate and butyrate and other fermentation metabolites such as lactate not only act as substrate for bacterial cross-feeding and as mediators in microbe-host interactions but also confer antimicrobial activity, which has received considerably less attention in the past research. It was the aim of this study to investigate the nutritional-microbial interactions that contribute to the development of infant gut microbiota with a focus on human milk oligosaccharide (HMO) fermentation. Infant fecal microbiota composition, fermentation metabolites and milk composition were analyzed from 69 mother-infant pairs of the Swiss birth cohort Childhood AlleRgy nutrition and Environment (CARE) at three time points depending on breastfeeding status defined at the age of 4 months, using quantitative microbiota profiling, HPLC-RI and 1H-NMR. We conducted in vitro fermentations in the presence of HMO fermentation metabolites and determined the antimicrobial activity of lactate and acetate against major Clostridiaceae and Peptostreptococcaceae representatives. Our data show that fucosyllactose represented 90% of the HMOs present in breast milk at 1- and 3-months post-partum with fecal accumulation of fucose, 1,2-propanediol and lactate indicating fermentation of HMOs that is likely driven by Bifidobacterium. Concurrently, there was a significantly lower absolute abundance of Peptostreptococcaceae in feces of exclusively breastfed infants at 3 months. In vitro, lactate inhibited strains of Peptostreptococcaceae. Taken together, this study not only identified breastfeeding dependent fecal microbiota and metabolite profiles but suggests that HMO-derived fermentation metabolites might exert an inhibitory effect against selected gut microbes.
- Keywords
- Exclusively breastfeeding, HMO fermentation metabolites, Peptostreptococcaceae, gut microbiota, lactate,
- MeSH
- Acetates metabolism MeSH
- Anti-Infective Agents * metabolism MeSH
- Clostridiales metabolism MeSH
- Child MeSH
- Feces microbiology MeSH
- Fermentation MeSH
- Infant MeSH
- Breast Feeding MeSH
- Lactic Acid metabolism MeSH
- Humans MeSH
- Milk, Human chemistry MeSH
- Oligosaccharides metabolism MeSH
- Gastrointestinal Microbiome * MeSH
- Check Tag
- Child MeSH
- Infant MeSH
- Humans MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Acetates MeSH
- Anti-Infective Agents * MeSH
- Lactic Acid MeSH
- Oligosaccharides MeSH
Dietary plant glucosides are phytochemicals whose bioactivity and bioavailability can be modified by glucoside hydrolase activity of intestinal microbiota through the release of acylglycones. Bifidobacteria are gut commensals whose genomic potential indicates host-adaption as they possess a diverse set of glycosyl hydrolases giving access to a variety of dietary glycans. We hypothesized bifidobacteria with β-glucosidase activity could use plant glucosides as fermentation substrate and tested 115 strains assigned to eight different species and from different hosts for their potential to express β-glucosidases and ability to grow in the presence of esculin, amygdalin, and arbutin. Concurrently, the antibacterial activity of arbutin and its acylglycone hydroquinone was investigated. Beta-glucosidase activity of bifidobacteria was species specific and most prevalent in species occurring in human adults and animal hosts. Utilization and fermentation profiles of plant glucosides differed between strains and might provide a competitive benefit enabling the intestinal use of dietary plant glucosides as energy sources. Bifidobacterial β-glucosidase activity can increase the bioactivity of plant glucosides through the release of acylglycone.
- Keywords
- amygdalin, antibacterial activity, arbutin, bifidobacteria, esculin, hydroquinone, β-glucosidase,
- Publication type
- Journal Article MeSH
Mucus production is initiated before birth and provides mucin glycans to the infant gut microbiota. Bifidobacteria are the major bacterial group in the feces of vaginally delivered and breast milk-fed infants. Among the bifidobacteria, only Bifidobacterium bifidum is able to degrade mucin and to release monosaccharides which can be used by other gut microbes colonizing the infant gut. Eubacterium hallii is an early occurring commensal that produces butyrate and propionate from fermentation metabolites but that cannot degrade complex oligo- and polysaccharides. We aimed to demonstrate that mucin cross-feeding initiated by B. bifidum enables growth and metabolite formation of E. hallii leading to short-chain fatty acid (SCFA) formation. Growth and metabolite formation of co-cultures of B. bifidum, of Bifidobacterium breve or Bifidobacterium infantis, which use mucin-derived hexoses and fucose, and of E. hallii were determined. Growth of E. hallii in the presence of lactose and mucin monosaccharides was tested. In co-culture fermentations, the presence of B. bifidum enabled growth of the other strains. B. bifidum/B. infantis co-cultures yielded acetate, formate, and lactate while co-cultures of B. bifidum and E. hallii formed acetate, formate, and butyrate. In three-strain co-cultures, B. bifidum, E. hallii, and B. breve or B. infantis produced up to 16 mM acetate, 5 mM formate, and 4 mM butyrate. The formation of propionate (approximately 1 mM) indicated cross-feeding on fucose. Lactose, galactose, and GlcNAc were identified as substrates of E. hallii. This study shows that trophic interactions of bifidobacteria and E. hallii lead to the formation of acetate, butyrate, propionate, and formate, potentially contributing to intestinal SCFA formation with potential benefits for the host and for microbial colonization of the infant gut. The ratios of SCFA formed differed depending on the microbial species involved in mucin cross-feeding.
- Keywords
- Bifidobacterium, Cross-feeding, Eubacterium hallii, Mucin, Propionate,
- MeSH
- Bifidobacterium growth & development isolation & purification metabolism MeSH
- Adult MeSH
- Eubacterium growth & development isolation & purification metabolism MeSH
- Feces microbiology MeSH
- Fermentation MeSH
- Infant MeSH
- Breast Feeding MeSH
- Fatty Acids, Volatile metabolism MeSH
- Humans MeSH
- Mucins metabolism MeSH
- Intestines microbiology MeSH
- Gastrointestinal Microbiome MeSH
- Animals MeSH
- Check Tag
- Adult MeSH
- Infant MeSH
- Humans MeSH
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Fatty Acids, Volatile MeSH
- Mucins MeSH