In our study Blon_2016 showed upregulation above the basal expression level on 3FL, but not on 2FL in the type strain, while Blon_2334 showed upregulation on 2FL but not 3FL in Bi-26 (Fig. Upregulation of the L-fucose utilization genes in the HMO-1 cluster in Bi-26, but not in ATCC 15697 is another indication of a regulatory adaptation to preferential utilization of small fucosylated HMOs by Bi-26. Verdel-Aranda, K., Lopez-Cortina, S. T., Hodgson, D. A. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: Mechanisms and implications. https://doi.org/10.1093/bioinformatics/btx364 (2017). The differences in the pyruvate metabolism detected in this study between the Bi-26 and the type strain likely explain the increased growth of Bi-26 on FLs and underscore specific adaptation of this B. infantis strain to the utilization of small fucosylated HMOs. 7A). PubMed FEBS J. Consideration of the full clinical evidence for B. infantis use in pediatric nutrition is critical to better understand its potential impacts on infant health and development. All growth experiments were conducted in triplicate in Hungate tubes with 5mL of mBasal media supplemented with 2% (w/v) of each carbon source and an initial inoculum of 0.05 optical density at 600nm (OD600). The resistome is the collection of all the antibiotic resistance genes, including those associated with pathogenic bacteria, non-pathogenic antibiotic producing bacteria, and all other resistance genes [60]. Whats normal? All tubes were incubated at 37C for 24h. Optical density readings were taken every 12h for 24h. The initial and final pH was measured using Thermo Scientifics Orion star A211 pH meter. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. 5E, about 10mM of that was excreted as 1,2-PD, indicating that about a third of available fucose was catabolized by Bi-26 to 1,2-PD and pyruvate. Ser. Kwak MJ, Kwon SK, Yoon JK, Song JY, Seo JG, Chung MJ, Kim JF. The excreted pyruvate levels were comparable to the 1,2-PD molar levels accumulated in the same samples (from 8 to 9.8mM for all FLs). Firstly, to determine overall differences we assessed the global patterns of transcription on Bi-26 and the type strain with principal component analysis (PCA). J. Biol. Most of the missing genes are transporter systems for various HMOs, which underscores the Bi-26 apparent preference for 2FL, 3FL, and DFL utilization. 2022 Aug 8;14(15):3239. doi: 10.3390/nu14153239. B., Raybould, H. E. & Mills, D. A. Oligosaccharide binding proteins from Bifidobacterium longum subsp. Kumar R, Tripathi AS, Sharma N, Singh G, Mohapatra L. Chin J Integr Med. Utilization of host-derived glycans by intestinal lactobacillus and Bifidobacterium species. infantis strains (Fig. Appl. This symbiotic relationship is an example of coevolution (humans and B. infantis) to protect the full term neonate and nourish a healthy gut microbiota prior to weaning (as reviewed [18]). PubMed In Bi-26 all three FL compounds demonstrated the same pattern of downregulation of competing HMO utilization genes. B. longum is a microaerotolerant, anaerobic bacterium susceptible to many antimicrobial drugs ( Table ). https://doi.org/10.1186/gb-2010-11-10-r106 (2010). Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Human milk is recognized as the optimal food source for infant nutrition, providing the infant with the needed macronutrients, micronutrients and growth promoting factors needed for infant development, with its composition changing with age or needs of the infant1,2. In Bi-26, levels of 1,2-PD began to rise during the T2 timepoint (Supplemental Fig. Typically, fucosylated HMOs make up the majority (>40%) of the total HMOs found in breast milk unless the milk is derived from non-secretor and/or Lewis negative mothers8,9,11. National Library of Medicine 28, 975986. Species: Bifidobacterium infantis - LPSN USA 105, 1896418969. Galacto- and Fructo-oligosaccharides Utilized for Growth by Cocultures of Bifidobacterial Species Characteristic of the Infant Gut. In addition to their role in the gut, SCFA produced by B. infantis can enter circulation and directly affect the adipose tissue, lungs, brain, and liver, inducing overall beneficial metabolic effects [31]. Hooper, L. V., Xu, J., Falk, P. G., Midtvedt, T. & Gordon, J. I. However, L-fucose accumulation in the spent medium during the B. infantis growth on fucosylated HMOs has been reported in the literature, even if in passing24,33,60. Bifidobacterium Longum Subsp. Infantis - an overview - ScienceDirect 4B) compared to the type strain in all cases but lactose and fucose. Half of the SBPs were determined to bind mammalian glycans, including various types of HMOs44. 68, 18251829. https://doi.org/10.1128/MMBR.00036-17 (2017). 2020 May 28;12(6):1581. doi: 10.3390/nu12061581. Bosom Buddies: The Symbiotic Relationship Between Infants and Bifidobacterium longum ssp. It was based on the alignment of the concatenated amino acid and nucleotide sequences of 500 core proteins families. The probiotic strains Bifidobacterium longum subsp. Overall the two strains displayed different growth rates, pH, and 24-h cell density for all the FLs tested, with Bi-26 displaying slightly better utilization of all three FL compounds. 2016 Oct;39(7):429-439. doi: 10.1016/j.syapm.2016.07.004. This transposase is not present in Bi-26, but present in the type strain and several other strains of the subspecies. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Figure2 illustrates the current limited understanding of the concurrent assimilation of the FLs constituents L-fucose and lactose. BZ, SG, KCE, DN, SKS, BV, and CB are all employees or supported by DuPont Nutrition and Biosciences, which manufactures and sells Bifidobacterium longum subsp. Significantly different growth profiles demonstrated by Bi-26 and ATCC15697 on some substrates (e.g. 8, 239252. Children supplemented with M63 showed a significant improvement of symptom score of allergic rhinitis and asthma. Preclinical models, including the necrotizing enterocolitis (NEC) model, have demonstrated that B. infantis could potentially decrease intestinal permeability and increase stabilization of tight junction proteins [28,34]. Clipboard, Search History, and several other advanced features are temporarily unavailable. The .gov means its official. LNB-GNB cluster (Blon_0875Blon_0885) encodes an ABC transporter with solute binding subunit Blon_0883 specific for LNB as well as GNB and three enzymes of hexosamine metabolism. However, from out earlier work24 we know that at least a part of it is excreted by Bi-26 as L-fucose during growth on 2FL24 and that the amounts of 1,2-PD and L-fucose accumulating in the spent medium inversely correlated under these conditions (not shown). In this regard, the sharp increase in acetate and formate levels over lactate in ATCC 15697 (especially during growth on DFL) is likely due to increased conversion of the fucose-derived pyruvate into acetyl phosphate and formate. Our strain of interest, Bi-26, clusters in a separate sub-clade from the type strain. 1), and the terminal concentration of 1,2-PD was twice as high in Bi-26 as compared to the type strain (Fig. The recent advancements of 'omics techniques have facilitated the genetic and functional studies of different gut microbiota members. LoCascio R.G., Desai P., Sela D.A., Weimer B., Mills D.A. The authors would like to thank Stuart Huntley for the assembly and annotation of the Bifidobacterium longum subsp. Keywords: 18, 298307. Bunesova, V., Lacroix, C. & Schwab, C. Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense. Butyrate production from oligofructose fermentation by the human faecal flora: What is the contribution of extracellular acetate and lactate?. Samples were vortexed, and analysis was performed using a 1200 HPLC system (Agilent) with Refractive Index and Ultraviolet detectors. https://doi.org/10.1021/bp0257426 (2003). 1. has been a consultant for Mead Johnson Nutrition. Switching to pyruvate excretion as an additional fermentation end product under these conditions could be a valuable strategy of energy generation. B. infantis preferentially consumes smaller HMO species (degree of polymerization <7) which are consistently produced over the course of lactation and represent the bulk of HMO present in pooled milk samples [27]. Andrs J.D., Manzano S., Garca C., Rodrguez J.M., Espinosa-Martos I., Jimnez E. Modulatory effect of three probiotic strains on infants gut microbial composition and immunological parameters on a placebo-controlled, double-blind, randomised study. Bifidobacterium infantis ( B. infantis) is a "friendly" strain of bacteria. infantis that encodes specific enzymes for the metabolism of human milk oligosaccharides suggests a specific ecological adaptation. Bookshelf We first measured the secretion of fermentation end products such as formate, lactate, and acetate. Sela D.A., Li Y., Lerno L., Wu S., Marcobal A.M., German J.B., Chen X., Lebrilla C.B., Mills D.A. Stool samples were collected through PND 60. In B. breve UCC2003 the substrate utilization without growth phenotype was observed with L-fucose as sole carbohydrate source. Microbiol. We then created a smaller representative core genome tree for the B. longum species (Fig. Full article: Bifidobacterium infantis 35624 and other probiotics in 2, 94. https://doi.org/10.3389/fcimb.2012.00094 (2012). PEG with or without added probiotics was equally effective and safe in the treatment of children with chronic constipation. Glycosci. ), 3University College London, Great Ormond Street, London WC1N 3JH, UK, 4Division of Pediatric Gastroenterology, Indiana University School of Medicine, Indianapolis, IN 46202, USA, 5Boston Childrens Hospital, Gastroenterology, Boston, MA 02115, USA; ude.dravrah.snerdlihc@foohrednaV.noJ. Acids Res. As in several other studies listed in our review, the associated benefits cannot be exclusively attributed to R003 alone. Emerg. PubMed Article Nutrients. longum, and B. kashiwanohense the capacity for uptake and catabolism of HMOs is limited to specific strains and to selected types of HMOs18,30,51, in B. infantis strong growth on a wide range of HMOs is considered characteristic of the entire subspecies20,52,53. In particular, Bifidobacterium longum subspecies infantis (B. infantis) is well adapted to the infant gut and has co-evolved with the mother-infant dyad and gut microbiome, in part due to its ability to consume complex carbohydrates found in human milk. suis type strain LMG 21814, assuming all other genomes to fall into B. longum subsp. infantis Bi-26, 2FL and 3FL. The .gov means its official. Article Lack of differences in alpha diversity between Control and EVC001 is consistent with previous reports on breast-fed infants. 7A) indicates that these type 1 HMOs could in fact be consumed by Bi-26 in the presence of other intestinal bacteria capable of extracellular HMO degradation to LNB or other constituents44,46,47. In Bi-26 the transporter Blon_2175-2177 is missing, while the remainder of the locus is downregulated to the same extent by all three species of fucosyllactose. Google Scholar. Daz R, Torres-Miranda A, Orellana G, Garrido D. Microorganisms. However, B. longum is composed of three subspecies, two of which are represented in the bowel microbiota (B. longum subsp. 100, 78257833. longum and B. bifidum, with B. pseudocatenulatum, B. longum subsp. The suppressor (AERS-2mm) was set to 38mA. 74, 298303. These genes showed transcriptional changes of lesser degree or none compared to the transport systems. Bifidobacteria are a group of bacteria called probiotics that normally live in your intestines and stomach. Disclaimer. Henrick and colleagues postulated that loss of Bifidobacterium spp. A comparison of two probiotic strains of bifidobacteria in premature infants. Mother/infant dyads (n = 80) were randomized by parallel assignment to either lactation support (LS; Control) or LS + EVC001 (Evolve Biosystems, Davis, CA) over a 21-day feeding period [47]. Lauer, E. & Kandler, O. In contrast, Bi-26 employs a different strategy to dispose of the fucose-derived pyruvate: namely, via its excretion and dissipation to (R )-acetoin and/or intermediates of branched-chain amino acid biosynthesis (Fig. One month after discontinuing feeding EVC001, stool count of EVC001 persisted and was significantly higher compared to the control group [36]. Differential expression of important genes in Bi-26 and the type strain grown on 2FL, 3FL, or DFL is shown in Fig. Rep. 5, 13517. https://doi.org/10.1038/srep13517 (2015). An external calibration curve was used to calculate the concentration of formic acid in the samples using linear regression. In the type strain only 3FL demonstrated the same level of regulatory capacity, while 2FL inhibited a smaller number of genes (Fig. Pickard, J. M. et al. Accurate sampling is essential for comparison of cell growth and physiology between two different strains grown on 6 different carbon sources. Chichlowski M, Shah N, Wampler JL, Wu SS, Vanderhoof JA. B. infantis demonstrates growth in vitro using HMO as the sole carbon source, reaching a cell density 3-fold higher than B. longum subsp. Gotoh, A. et al. Google Scholar. The column temperature was maintained at 35C with a flow rate of 0.25mL/min. Ravcheev, D. A. infantis physiology. B. infantis and its human host have a symbiotic relationship that protects the preterm or . Overall, supplementation with a probiotic mix, which included R0033, significantly decreased the risk of occurrence of common infectious diseases in children. HHS Vulnerability Disclosure, Help 1) with 30 of the identified B. infantis genomes with acceptable quality, all publicly available genomes that clustered with B. longum subsp. Efficacy of Bifidobacterium infantis 35624 in patients with irritable In addition, stool HMO from PND 6 to 29 were significantly lower (suggesting increased bifidobacteria metabolism) in the EVC001 group compared to the control group; acetate and lactate were significantly higher in the EVC001 vs. the control group. 96, 570577 (2006). Federal government websites often end in .gov or .mil. Wattham, R. PATRIC Database. These clusters are displayed in Fig. While the type strain is a generalist, that was shown to consume different types of HMOs simultaneously and equally well without a preference for any neutral or fucosylated HMO8,22,33,52, we propose that Bi-26 is adapted to quickly internalize small fucosylated HMOs. Ecol. 3D). 2002, Bifidobacterium infantis Reuter 1963 (Approved Lists 1980) is a later heterotypic synonym of Bifidobacterium longum Reuter 1963 (Approved Lists 1980). government site. 64, 8399 (2012). infantis in purple, with the Bi-26 clade highlighted in deeper shade. Both strains were tested for growth on glucose, lactose, 2-fucosyllactose (2FL), 3-fucosyllactose (3FL), di-fucosyllactose (DFL), or fucose as the sole source of carbon. 86, 731747. 3D). They are ubiquitous inhabitants of the gastrointestinal tract [2] [3] though strains have been isolated from the vagina [4] and mouth ( B. dentium) of mammals, including humans. was similar between groups; however, B. infantis was significantly higher in the CECT7210 group. https://doi.org/10.3945/ajcn.116.139980 (2017). https://doi.org/10.1097/mpg.0000000000000752 (2015). are employed by the study sponsor, Mead Johnson Nutrition. Ishizeki S., Sugita M., Takata M., Yaeshima T. Effect of administration of bifidobacteria on intestinal microbiota in low-birth-weight infants and transition of administered bifidobacteria: A comparison between one-species and three-species administration. The genome sequence of Bifidobacterium longum subsp. infantis reveals 6, Supplemental Fig. https://doi.org/10.1016/j.ymben.2014.08.003 (2014). The universal importance of bifidobacteria in human microbiota and gastrointestinal (GI) health from infancy to advanced years (as reviewed [1]), including the critical role of genus Bifidobacterium in the process of immune maturation early in life (as reviewed [2]), have been detailed in a wealth of literature. Front. It's a type of lactic acid bacteria found in the same group as Lactobacillus. As new ingredients become available, safety and suitability must be assessed in preclinical and clinical studies. The central position of pyruvate in fucosyllactose utilization by B. infantis prompted us to analyze this compound along with the classic end fermentation products: acetate, lactate, and formate. Microb. Rev. Boronat, A. PLoS ONE. After autoclaving, we added filter-sterilized (0.2uM, PES membrane) 0.05% (w/v) L-cysteine HCl and 2% (w/v) of the indicated carbon source. 200L of metabolite sample was aliquoted into an HPLC vial with an insert (minimum 100L to avoid mis-injections) and ran without dilution. Colonization and succession within the human gut microbiome by archaea, bacteria, and microeukaryotes during the first year of life. Term infants were enrolled (n = 106, newborn) in a DBRCT; participants received a control IF or IF with an added probiotic mix of B. infantis BT1, B. bifidum BF3, B. breve BR3, and B. longum BG7 (total 10 million CFU/g) through 12 months of age to measure fecal microbiota diversity and composition [57]. longum subspecies available in PATRIC database. The two most dominant Bifidobacterium species were Bifidobacterium longum subsp. 19, 672675. 60, 825833. 79, 76287638. Bergmann K.R., Liu S.X.L., Tian R., Kushnir A., Turner J.R., Li H.L., Chou P.M., Weber C.R., De Plaen I.G. *p value0.05; **p value0.006; ***p value0.0002. Higgins, C. F. ABC transporters: Physiology, structure and mechanismAn overview. The data for all timepoints for Bi-26 is shown in Supplemental Fig. Likewise, in our study no significant growth on L-fucose as the sole carbon source was observed for both strains (Fig. contributed to the drafting, editing, and revision of this review. Use the Previous and Next buttons to navigate the slides or the slide controller buttons at the end to navigate through each slide. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Paired-end RNA sequencing data were subsampled to 5 million reads per sample and interleaved into a single file using BBmerge version 1.1.3 with default settings within Geneious Prime version 2020.0.5 (Aukland, New Zealand). End-metabolites of bifidobacteria and other lactic acid bacteria (LABs) in human gut have been shown to serve as substrates for secondary degraders such as butyrate-producing colonic bacteria72,73,74,75,76. In this study we used comparative genomics, metabolite analysis and transcriptomics to analyze the growth of the type strain and B. infantis strain Bi-26 (Bi-26) on 2FL, 3FL, and DFL (FLs) as sole carbon sources. Bioinformatics 30, 13121313. 2, 7B). Feeding-related GI adverse events were significantly lower in infants receiving M63. 2016 Oct 26;16(1):248. doi: 10.1186/s12866-016-0867-4. Agarwala, R. et al. This site needs JavaScript to work properly. Finally, in stool samples from the same cohort, significantly lower calprotectin and proinflammatory cytokines were reported in infants receiving EVC001 [50] suggesting lower enteric inflammation. Duncan, S. H. et al. Environ. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., et al. In continuation of analyses conducted on the same cohort, significantly more stool N-glycans (specific complex carbohydrates released from milk glycoproteins and available for select use by B. infantis) were measured in stool samples from the EVC001 group. doi: 10.1007/s12263-010-0206-6. Total number of DEGs is shown on the left (blue bars) for each of the conditions while the number of shared genes per condition (shown by the connected dots), is shown above the black bars (significance cut-offs: BenjaminiHochberg adjusted p value<0.05; log2>1.5). Over 200 structurally distinct HMOs have been identified7 with chain lengths from 3 to 15 carbohydrate units, composed of five monosaccharides: glucose, galactose, N-acetylglucosamine, fucose, and N-acetylneuraminic acid (also known as sialic acid). In this study we show that at least two distinct strategies for FL utilization are evident within the B. infantis subspecies. Clinical outcomes, including length of hospital stay did not differ between groups. 16 A Bifidobacterium infantis strain (B.infantis 35624, Align, Proctor and Gamble, Cincinnati, OH) was . Google Scholar. J. Pediatr. Bifidobacterium longumspp. The site is secure. While both genomes have a similar number of coding genes, only 80% of these CDSs are orthologous (~1960 genes). Hall, Bryan Zabel, Christian Clement Yde, Wesley Morovic, Mary OConnell Motherway, Frances OBrien, Douwe van Sinderen, Michael Jakob Pichler, Chihaya Yamada, Maher Abou Hachem, Eva M. Moya-Gonzlvez, Antonio Rubio-del-Campo, Mara J. Yebra, Antonio Rubio-del-Campo, Cristina Alcntara, Mara J. Yebra, Scientific Reports A fold change 1.5-fold and BenjaminiHochberg adjusted p value<0.05 were considered for statistical significance. infantis Bi-26 (Bi-26) and the type strain. Schwab, C. et al. ADS 77, 229235. Also, of note is a very low number of DEGs evident in the type strain transcriptome on glucose, drastically lower than any other transcriptomes generated in this study (Fig. Microbiol. Succession of microbial consortia in the developing infant gut microbiome. 194, 55885593. Here, the mechanisms of the Bifidobacterium longum in the treatment of IBD were summarized based on previous cell and animal studies and . Falony, G., Calmeyn, T., Leroy, F. & De Vuyst, L. Coculture fermentations of Bifidobacterium species and Bacteroides thetaiotaomicron reveal a mechanistic insight into the prebiotic effect of inulin-type fructans. Additionally, with the rise in caesarian births and decreasing diversity in the microbiome82, supplementation with B. infantis strains utilizing different metabolic strategies of fucosyllactose utilization may be beneficial to infants that would not be exposed to it naturally. Considering the late onset of both processes, they appear to be a specific adaptation in Bi-26 for maintaining ATP generation when the classic fermentation pathways slow down, as the excretion of their end products (acetate, lactate, formate, ethanol) is arrested by significant accumulation of these compounds in the spent medium. Other study groups included L. helveticus and B. bifidum. Importantly, Blon_22022204 has a wider substrate specificity than Blon_03410343. Additional timepoints for Bi-26 were taken at OD600 of 0.40.6 (T2) and OD600 of 1.0 (T3) to further characterize how FLs are metabolized (Supplemental Fig. Furthermore, DFL did not inhibit any genes in the type strain (Fig. Front. The pH was adjusted to 6.4. Bethesda, MD 20894, Web Policies These core oligosaccharides are often fucosylated by adding fucose (via 12/3/4 linkages) and/or sialylated by adding sialic acid via 23/6 linkages5,8,9. Bifidobacterium longum - Probiotic Bacteria with a Long List of Health Benefits. J.A.V. Lactation and Intestinal Microbiota: How Early Diet Shapes the Infant Gut. & Prieto, P. A. Instead, 2FL, 3FL, and DFL induced the expression of alternative operons, distinct from the HMO-1 cluster (clusters Fucosyllactose-1, 2, and 3 in Fig. 1E), we also observed an activation of several pathways of pyruvate dissipation in the DFL transcriptome of this strain, especially at the T3 timepoint (Fig. & Thiele, I. & Tannock, G. W. Bifidobacterium bifidum ATCC 15696 and Bifidobacterium breve 24b metabolic interaction based on 2-O-fucosyl-lactose studied in steady-state cultures in a freter-style chemostat. Genus Bifidobacterium was originally isolated from the stool of breastfed infants in 1899, by Henri Tissier (as reviewed [2]). 5D) indicate that about half of the pyruvate generated in this process was excreted and not incorporated into the biomass. Di Gioia, D., Aloisio, I., Mazzola, G. & Biavati, B. Bifidobacteria: Their impact on gut microbiota composition and their applications as probiotics in infants. https://doi.org/10.1038/s41598-020-72792-z, DOI: https://doi.org/10.1038/s41598-020-72792-z. 7). Neonatal diet alters fecal microbiota and metabolome profiles at different ages in infants fed breast milk or formula. Sela D.A., Mills D.A. . The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. Secondary outcomes included incidence of infection, salivary IgA levels, stool microbiota, infant growth, and tolerance measures. Early probiotic supplementation with B. infantis in breastfed infants Once internalized, the small fucosylated HMOs are processed by glycosyl hydrolases, which are represented by multiple genes in all B. infantis genomes. Fucose and lactose standards (99% purity) were obtained from Sigma-Aldrich.
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