Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27782805
PubMed Central
PMC5080750
DOI
10.1186/s12866-016-0867-4
PII: 10.1186/s12866-016-0867-4
Knihovny.cz E-zdroje
- Klíčová slova
- 1,2 propanediol, Bifidobacterium, HMOs, L-fucose, fucosyllactose,
- MeSH
- alfa-L-fukosidasa klasifikace genetika metabolismus MeSH
- beta-galaktosidasa metabolismus MeSH
- Bifidobacterium longum enzymologie genetika metabolismus MeSH
- Bifidobacterium enzymologie genetika metabolismus MeSH
- DNA bakterií genetika MeSH
- feces mikrobiologie MeSH
- fukosa metabolismus MeSH
- genom bakteriální MeSH
- kojenec MeSH
- kyseliny mastné těkavé metabolismus MeSH
- kyseliny sialové metabolismus MeSH
- laktosa analogy a deriváty metabolismus MeSH
- lidé MeSH
- mateřské mléko metabolismus MeSH
- metabolické sítě a dráhy MeSH
- oligosacharidy metabolismus MeSH
- propylenglykol metabolismus MeSH
- RNA ribozomální 16S genetika MeSH
- sekvence nukleotidů MeSH
- střeva mikrobiologie MeSH
- trisacharidy metabolismus MeSH
- Check Tag
- kojenec MeSH
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- 2'-fucosyllactose MeSH Prohlížeč
- 3'-fucosyllactose MeSH Prohlížeč
- 3'-sialyllactose MeSH Prohlížeč
- alfa-L-fukosidasa MeSH
- beta-galaktosidasa MeSH
- DNA bakterií MeSH
- fukosa MeSH
- kyseliny mastné těkavé MeSH
- kyseliny sialové MeSH
- lacto-N-neotetraose MeSH Prohlížeč
- laktosa MeSH
- N-acetylneuraminoyllactose MeSH Prohlížeč
- oligosacharidy MeSH
- propylenglykol MeSH
- RNA ribozomální 16S MeSH
- trisacharidy MeSH
BACKGROUND: Human milk oligosaccharides (HMOs) are one of the major glycan source of the infant gut microbiota. The two species that predominate the infant bifidobacteria community, Bifidobacterium longum subsp. infantis and Bifidobacterium bifidum, possess an arsenal of enzymes including α-fucosidases, sialidases, and β-galactosidases to metabolise HMOs. Recently bifidobacteria were obtained from the stool of six month old Kenyan infants including species such as Bifidobacterium kashiwanohense, and Bifidobacterium pseudolongum that are not frequently isolated from infant stool. The aim of this study was to characterize HMOs utilization by these isolates. Strains were grown in presence of 2'-fucosyllactose (2'-FL), 3'-fucosyllactose (3'-FL), 3'-sialyl-lactose (3'-SL), 6'-sialyl-lactose (6'-SL), and Lacto-N-neotetraose (LNnT). We further investigated metabolites formed during L-fucose and fucosyllactose utilization, and aimed to identify genes and pathways involved through genome comparison. RESULTS: Bifidobacterium longum subsp. infantis isolates, Bifidobacterium longum subsp. suis BSM11-5 and B. kashiwanohense strains grew in the presence of 2'-FL and 3'- FL. All B. longum isolates utilized the L-fucose moiety, while B. kashiwanohense accumulated L-fucose in the supernatant. 1,2-propanediol (1,2-PD) was the major metabolite from L-fucose fermentation, and was formed in equimolar amounts by B. longum isolates. Alpha-fucosidases were detected in all strains that degraded fucosyllactose. B. longum subsp. infantis TPY11-2 harboured four α-fucosidases with 95-99 % similarity to the type strain. B. kashiwanohense DSM 21854 and PV20-2 possessed three and one α-fucosidase, respectively. The two α-fucosidases of B. longum subsp. suis were 78-80 % similar to B. longum subsp. infantis and were highly similar to B. kashiwanohense α-fucosidases (95-99 %). The genomes of B. longum strains that were capable of utilizing L-fucose harboured two gene regions that encoded enzymes predicted to metabolize L-fucose to L-lactaldehyde, the precursor of 1,2-PD, via non-phosphorylated intermediates. CONCLUSION: Here we observed that the ability to utilize fucosyllactose is a trait of various bifidobacteria species. For the first time, strains of B. longum subsp. infantis and an isolate of B. longum subsp. suis were shown to use L-fucose to form 1,2-PD. As 1,2-PD is a precursor for intestinal propionate formation, bifidobacterial L-fucose utilization may impact intestinal short chain fatty acid balance. A L-fucose utilization pathway for bifidobacteria is suggested.
Zobrazit více v PubMed
Bottacini F, Medini D, Pavesi A, Turroni F, Foroni E, Riley D, et al. Comparative genomics of the genus Bifidobacterium. Microbiol-Sgm. 2010;156:3243–54. doi: 10.1099/mic.0.039545-0. PubMed DOI
Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract (vol 99, pg 14422, 2002) Proc Natl Acad Sci U S A. 2005;102:9430. PubMed PMC
Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A. 2008;105:18964–9. doi: 10.1073/pnas.0809584105. PubMed DOI PMC
Duranti S, Turroni F, Lugli GA, Milani C, Viappiani A, Mangifesta M, et al. Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22 L. Appl Environ Microbiol. 2014;80:6080–90. doi: 10.1128/AEM.01993-14. PubMed DOI PMC
Milani C, Lugli GA, Duranti S, Turroni F, Bottacini F, Mangifesta M, et al. Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl Environ Microbiol. 2014;80:6290–302. doi: 10.1128/AEM.02308-14. PubMed DOI PMC
Pokusaeva K, Fitzgerald GF, van Sinderen D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 2011;6:285–306. doi: 10.1007/s12263-010-0206-6. PubMed DOI PMC
Sun Z, Zhang W, Guo C, Yang X, Liu W, Wu Y, et al. Comparative genomic analysis of 45 type strains of the genus Bifidobacterium: a snapshot of its genetic diversity and evolution. PLoS One. 2015;10:e0117912. doi: 10.1371/journal.pone.0117912. PubMed DOI PMC
Bottacini F, Ventura M, Sinderen D, Motherway MOC. Diversity, ecology and intestinal function of bifidobacteria. Microbiol Cell Fact. 2014;13:1024. doi: 10.1186/1475-2859-13-S1-S4. PubMed DOI PMC
Liu S, Ren F, Zhao L, Jiang L, Hao Y, Jin J, et al. Starch and starch hydrolysates are favorable carbon sources for Bifidobacteria in the human gut. BMC Microbiol. 2015;15:54. doi: 10.1186/s12866-015-0362-3. PubMed DOI PMC
Rockova S, Rada V, Nevoral J, Marsik P, Vlkova E, Bunesova V. Inter-species differences in the growth of bifidobacteria cultured on human milk oligosaccharides. Folia Microbiol. 2012;57:321–4. doi: 10.1007/s12223-012-0134-5. PubMed DOI
LoCascio RG, Desai P, Sela DA, Weimer B, Mills DA. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl Environ Microbiol. 2010;76:7373–81. doi: 10.1128/AEM.00675-10. PubMed DOI PMC
Turroni F, Duranti S, Bottacini F, Guglielmetti S, Van Sinderen D, Ventura M. Bifidobacterium bifidum as an example of a specialized human gut commensal. Front Microbiol. 2014;5:437. doi: 10.3389/fmicb.2014.00437. PubMed DOI PMC
Kunz C, Rudloff S, Baier W, Klein N, Strobel S. Oligosaccharides in human milk. Structural, functional, and metabolic aspects. Annu Rev Nutr. 2000;20:699–722. doi: 10.1146/annurev.nutr.20.1.699. PubMed DOI
Egan M, Motherway MOC, Kilcoyne M, Kane M, Joshi L, Ventura M, van Sinderen D. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol. 2014;14:282. doi: 10.1186/s12866-014-0282-7. PubMed DOI PMC
Ruiz-Moyano S, Totten SM, Garrido DA, Smilowitz JT, Bruce German J, Lebrilla CB, et al. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol. 2013;79:6040–9. doi: 10.1128/AEM.01843-13. PubMed DOI PMC
Matsuki T, Yahagi K, Mori H, Matsumoto H, Hara T, Tajima S, et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun. 2016;7:11939. doi: 10.1038/ncomms11939. PubMed DOI PMC
de Vries W, Stouthamer AH. Pathway of glucose fermentation in relation to the taxonomy of bifidobacteria. J Bacteriol. 1967;93:574–6. PubMed PMC
Palframan RJ, Gibson GR, Rastall RA. Carbohydrate preferences of Bifidobacterium species isolated from the human gut. Curr Issues Intest Microbiol. 2003;4:71–5. PubMed
de Vries W, Stouthamer AH. Fermentation of glucose, lactose, galactose, mannitol, and xylose by bifidobacteria. J Bacteriol. 1968;96:472–8. PubMed PMC
Vazquez-Gutierrez P, Lacroix C, Jaeggi T, Zeder C, Zimmerman MB, Chassard C. Bifidobacteria strains isolated from stools of iron deficient infants can efficiently sequester iron. BMC Microbiol. 2015;15:3. doi: 10.1186/s12866-014-0334-z. PubMed DOI PMC
Morita H, Nakano A, Onoda H, Toh H, Oshima K, Takami H, et al. Bifidobacterium kashiwanohense sp nov., isolated from healthy infant faeces. Int J Syst Evol Microbiol. 2011;61:2610–5. doi: 10.1099/ijs.0.024521-0. PubMed DOI
Gavini F, Delcenserie V, Kopeinig K, Pollinger S, Beerens H, Bonaparte C, Upmann M. Bifidobacterium species isolated from animal feces and from beef and pork meat. J Food Prot. 2006;69:871–7. PubMed
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9. doi: 10.1093/molbev/mst197. PubMed DOI PMC
Aziz RK, Bartels D, Best A, DeJongh M, Disz T, Edwards RA, et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75. doi: 10.1186/1471-2164-9-75. PubMed DOI PMC
Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. Peer J Preprints. 2016;4:e1900v1.
Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC. CAZymes analysis toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology. 2010;20:1574–84. doi: 10.1093/glycob/cwq106. PubMed DOI
Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y. DbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2012;40:W445–51. doi: 10.1093/nar/gks479. PubMed DOI PMC
Turroni F, Bottacini F, Foroni E, Mulder I, Kim J-H, Zomer A, et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci U S A. 2010;107:19514–9. doi: 10.1073/pnas.1011100107. PubMed DOI PMC
Scott KP, Martin JC, Campbell G, Mayer CD, Flint HJ. Whole-genome transcription profiling reveals genes up-regulated by growth on fucose in the human gut bacterium “Roseburia inulinivorans”. J Bacteriol. 2006;188:4340–9. doi: 10.1128/JB.00137-06. PubMed DOI PMC
Boronat A, Aguilar J. Metabolism of L-fucose and L-rhamnose in Escherichia coli: differences in induction of propanediol oxidoreductase. J Bacteriol. 1981;147:181–5. PubMed PMC
Saxena RK, Anand P, Saran S, Isar J, Agarwal L. Microbial production and applications of 1,2-propanediol. Indian J Microbiol. 2010;50:2–11. doi: 10.1007/s12088-010-0017-x. PubMed DOI PMC
Crost EH, Tailford LE, Le Gall G, Fons M, Henrissat B, Juge N. Utilisation of Mucin Glycans by the Human Gut Symbiont Ruminococcus gnavus Is Strain-Dependent. PLoS One. 2013;8:e76341. doi: 10.1371/journal.pone.0076341. PubMed DOI PMC
Cocks GT, Aguilar J, Lin ECC. Evolution of L 1,2 propanediol catabolism in Escherichia coli by recruitment of enzymes for L fucose and L lactate metabolism. J Bacteriol. 1974;118:83–8. PubMed PMC
Garrido D, Ruiz-Moyano S, Lemay DG, Sela DA, German JB, Mills DA. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci Rep. 2015;5:13517. doi: 10.1038/srep13517. PubMed DOI PMC
Gänzle MG. Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr Opin Food Sci. 2015;2:106–17. doi: 10.1016/j.cofs.2015.03.001. DOI
Engels C, Ruscheweyh H-J, Beerenwinkel N, Lacroix C, Schwab C. The common gut microbe Eubacterium hallii also contributes to intestinal propionate formation. Front Microbiol. 2016;7:713. doi: 10.3389/fmicb.2016.00713. PubMed DOI PMC
Reichardt N, Duncan SH, Young P, Belenguer A, McWilliam Leitch C, Scott KP, et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J. 2014;8:1323–35. doi: 10.1038/ismej.2014.14. PubMed DOI PMC
Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 2014;12:661–72. doi: 10.1038/nrmicro3344. PubMed DOI
Morita H, Toh H, Nakano A, Oshima K, Takagi M, Suda W, et al. Complete Genome Sequence of Bifidobacterium kashiwanohense JCM 15439(T), Isolated from Feces from a Healthy Japanese Infant. Genome Announc. 2015;3:e00255–00215. doi: 10.1128/genomeA.00255-15. PubMed DOI PMC
Vazquez-Gutierrez P, Lacroix C, Chassard C, Klumpp J, Jans C, Stevens MJA. Complete and assembled genome sequence of Bifidobacterium kashiwanohense p V20–2, isolated from the feces of an anemic Kenyan infant. Genome Announc. 2015;3:e01467–01414. PubMed PMC
Sela DA, Garrido D, Lerno L, Wu S, Tan K, Eom HJ, et al. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl Environ Microbiol. 2012;78:795–803. doi: 10.1128/AEM.06762-11. PubMed DOI PMC
Becerra JE, Yebra MJ, Monedero V. An L-fucose operon in the probiotic Lactobacillus rhamnosus GG is involved in adaptation to gastrointestinal conditions. Appl Environ Microbiol. 2015;81:3880–8. doi: 10.1128/AEM.00260-15. PubMed DOI PMC
Stahl M, Friis LM, Nothaft H, Liu X, Li J, Szymanski CM, Stintzi A. L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A. 2011;108:7194–9. doi: 10.1073/pnas.1014125108. PubMed DOI PMC
Yew WS, Fedorov AA, Fedorov EV, Rakus JF, Pierce RW, Almo SC, Gerlt JA. Evolution of enzymatic activities in the enolase superfamily: L-fuconate dehydratase from Xanthomonas campestris. Biochemistry. 2006;45:14582–97. doi: 10.1021/bi061687o. PubMed DOI
Watanabe S, Makino K. Novel modified version of nonphosphorylated sugar metabolism - An alternative L-rhamnose pathway of Sphingomonas sp. FEBS J. 2009;276:1554–67. doi: 10.1111/j.1742-4658.2009.06885.x. PubMed DOI
Scapin G, Blanchard JS. Enzymology of bacterial lysine biosynthesis. Adv Enzymol Relat Areas Mol Biol. 1998;72:279–324. PubMed
Mucin Cross-Feeding of Infant Bifidobacteria and Eubacterium hallii