1,975
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Characterization of Bifidobacterium kashiwanohense that utilizes both milk- and plant-derived oligosaccharides

Article: 2207455 | Received 11 Oct 2022, Accepted 12 Apr 2023, Published online: 15 May 2023

References

  • Dogra S, Sakwinska O, Soh S-E, Ngom-Bru C, Brück WM, Berger B, Brüssow H, Lee YS, Yap F, Chong Y-S, et al. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. mBio. 2015;6: e02419-14. doi:10.1128/mBio.02419-14.
  • Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469:543–17. doi:10.1038/nature09646.
  • Björkstén B, Sepp E, Julge K, Voor T, Mikelsaar M. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol. 2001;108:516–520. doi:10.1067/mai.2001.118130.
  • Kalliomäki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001;107:129–134. doi:10.1067/mai.2001.111237.
  • Watanabe S, Narisawa Y, Arase S, Okamatsu H, Ikenaga T, Tajiri Y, Kumemura M. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol. 2003;111:587–591. doi:10.1067/mai.2003.105.
  • Duranti S, Milani C, Lugli GA, Mancabelli L, Turroni F, Ferrario C, Mangifesta M, Viappiani A, Sánchez B, Margolles A, et al. Evaluation of genetic diversity among strains of the human gut commensal Bifidobacterium adolescentis. Sci Rep. 2016;6:23971. doi:10.1038/srep23971.
  • Matsuki T, Yahagi K, Mori H, Matsumoto H, Hara T, Tajima S, Ogawa E, Kodama H, Yamamoto K, Yamada T, et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun. 2016;7:11939. doi:10.1038/ncomms11939.
  • Watanabe Y, Saito Y, Hara T, Tsukuda N, Aiyama-Suzuki Y, Tanigawa-Yahagi K, Kurakawa T, Moriyama-Ohara K, Matsumoto S, Matsuki T. Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract. ISME Commun. 2021;1:1–11. doi:10.1038/s43705-021-00066-4.
  • Bottacini F, Morrissey R, Esteban-Torres M, James K, van Breen J, Dikareva E, Egan M, Lambert J, van Limpt K, Knol J, et al. Comparative genomics and genotype-phenotype associations in Bifidobacterium breve. Sci Rep. 2018;8:10633. doi:10.1038/s41598-018-28919-4.
  • Duar RM, Casaburi G, Mitchell RD, Scofield LNC, Ortega Ramirez CA, Barile D, Henrick BM, Frese SA. Comparative genome analysis of Bifidobacterium longum subspinfantis Strains Reveals Variation in Human Milk Oligosaccharide Utilization Genes among Commercial Probiotics. Nutrients. 2020;12:3247. doi:10.3390/nu12113247.
  • Liu J, Li W, Yao C, Yu J, Zhang H. Comparative genomic analysis revealed genetic divergence between Bifidobacterium catenulatum subspecies present in infant versus adult guts. BMC Microbiol. 2022;22:158. doi:10.1186/s12866-022-02573-3.
  • Tarracchini C, Milani C, Lugli GA, Mancabelli L, Fontana F, Alessandri G, Longhi G, Anzalone R, Viappiani A, Turroni F, et al. Phylogenomic disentangling of the Bifidobacterium longum subsp. infantistaxon. Microb Genomics. 2021;7:000609. doi:10.1099/mgen.0.000609.
  • Kato K, Odamaki T, Mitsuyama E, Sugahara H, Xiao J, Osawa R. Age-related changes in the composition of gut bifidobacterium species. Curr Microbiol. 2017;74:987–995. doi:10.1007/s00284-017-1272-4.
  • Tsukuda N, Yahagi K, Hara T, Watanabe Y, Matsumoto H, Mori H, Higashi K, Tsuji H, Matsumoto S, Kurokawa K, et al. Key bacterial taxa and metabolic pathways affecting gut short-chain fatty acid profiles in early life. Isme J. 2021:1–17. doi:10.1038/s41396-021-00937-7
  • Odamaki T, Bottacini F, Kato K, Mitsuyama E, Yoshida K, Horigome A, Xiao J, van Sinderen D. Genomic diversity and distribution of Bifidobacterium longum subsp. longum across the human lifespan. Sci Rep. 2018;8:85. doi:10.1038/s41598-017-18391-x.
  • Nagara Y, Fujii D, Takada T, Sato-Yamazaki M, Odani T, Oishi K. Selective induction of human gut-associated acetogenic/butyrogenic microbiota based on specific microbial colonization of indigestible starch granules. Isme J. 2022;16:1–10. doi:10.1038/s41396-022-01196-w.
  • Saito Y, Shigehisa A, Watanabe Y, Tsukuda N, Moriyama-Ohara K, Hara T, Matsumoto S, Tsuji H, Matsuki T, Zhou N-Y. Multiple transporters and glycoside hydrolases are involved in arabinoxylan-derived oligosaccharide utilization in Bifidobacterium pseudocatenulatum. Appl Environ Microbiol. 2020;86: e01782-20. doi:10.1128/AEM.01782-20.
  • Duranti S, Turroni F, Lugli GA, Milani C, Viappiani A, Mangifesta M, Gioiosa L, Palanza P, van Sinderen D, Ventura M, et al. Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22L. Appl Environ Microbiol. 2014;80:6080–6090. doi:10.1128/AEM.01993-14.
  • Jung D-H, Seo D-H, Kim Y-J, Chung W-H, Nam Y-D, Park C-S. The presence of resistant starch-degrading amylases in Bifidobacterium adolescentis of the human gut. Int J Biol Macromol. 2020;161:389–397. doi:10.1016/j.ijbiomac.2020.05.235.
  • Sakanaka M, Gotoh A, Yoshida K, Odamaki T, Koguchi H, Xiao J, Kitaoka M, Katayama T. Varied pathways of infant gut-associated bifidobacterium to assimilate human milk oligosaccharides: prevalence of the gene set and its correlation with bifidobacteria-rich microbiota formation. Nutrients. 2020;12:71. doi:10.3390/nu12010071.
  • Hundshammer C, Minge O. In love with shaping you—influential factors on the breast milk content of human milk oligosaccharides and their decisive roles for neonatal development. Nutrients. 2020;12:3568. doi:10.3390/nu12113568.
  • Sakanaka M, Hansen ME, Gotoh A, Katoh T, Yoshida K, Odamaki T, Yachi H, Sugiyama Y, Kurihara S, Hirose J, et al. Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. Sci Adv. 2019;5:eaaw7696. doi:10.1126/sciadv.aaw7696.
  • Underwood MA, German JB, Lebrilla CB, Mills DA. Bifidobacterium longum subspecies infantis: champion colonizer of the infant gut. Pediatr Res. 2015;77:229–235. doi:10.1038/pr.2014.156.
  • Wagner A. Energy Constraints On The Evolution Of Gene Expression. Mol Biol Evol. 2005;22:1365–1374. doi:10.1093/molbev/msi126.
  • Katayama T, Sakuma A, Kimura T, Makimura Y, Hiratake J, Sakata K, Yamanoi T, Kumagai H, Yamamoto K. Molecular cloning and characterization of bifidobacterium bifidum 1,2-α-l-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol. 2004;186:4885–4893. doi:10.1128/JB.186.15.4885-4893.2004.
  • James K, Bottacini F, Contreras JIS, Vigoureux M, Egan M, Motherway MO, Holmes E, van Sinderen D. Metabolism of the predominant human milk oligosaccharide fucosyllactose by an infant gut commensal. Sci Rep. 2019;9:15427. doi:10.1038/s41598-019-51901-7.
  • Morita H, Nakano A, Onoda H, Toh H, Oshima K, Takami H, Murakami M, Fukuda S, Takizawa T, Kuwahara T, et al. Bifidobacterium kashiwanohense sp. nov., isolated from healthy infant faeces. Int J Syst Evol Microbiol. 2011;61:2610–2615. doi:10.1099/ijs.0.024521-0.
  • Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T, Kyrpides NC, Pukall R, Klenk H-P, Goodfellow M, Göker M. Genome-based taxonomic classification of the phylum actinobacteria. Front Microbiol. 2018;9:2007. doi:10.3389/fmicb.2018.02007.
  • Bunesova V, Lacroix C, Schwab C. Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense. BMC Microbiol. 2016;16:248. doi:10.1186/s12866-016-0867-4.
  • Freitas AC, Hill JE. Quantification, isolation and characterization of Bifidobacterium from the vaginal microbiomes of reproductive aged women. Anaerobe. 2017;47:145–156. doi:10.1016/j.anaerobe.2017.05.012.
  • Vazquez-Gutierrez P, Lacroix C, Chassard C, Klumpp J, Jans C, Stevens MJA. Complete and assembled genome sequence of Bifidobacterium kashiwanohense pv20-2, isolated from the feces of an anemic kenyan infant. Genome Announc. 2015;3: e01467-14. doi:10.1128/genomeA.01467-14.
  • Morita H, Toh H, Oshima K, Nakano A, Yamashita N, Iioka E, Arakawa K, Suda W, Honda K, Hattori M. Complete genome sequence of Bifidobacterium catenulatum JCM 1194T isolated from human feces. J Biotechnol. 2015;210:25–26. doi:10.1016/j.jbiotec.2015.06.415.
  • Duranti S, Lugli GA, Mancabelli L, Armanini F, Turroni F, James K, Ferretti P, Gorfer V, Ferrario C, Milani C, et al. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission. Microbiome. 2017;5:66. doi:10.1186/s40168-017-0282-6.
  • Poyet M, Groussin M, Gibbons SM, Avila-Pacheco J, Jiang X, Kearney SM, Perrotta AR, Berdy B, Zhao S, Lieberman TD, et al. A library of human gut bacterial isolates paired with longitudinal multiomics data enables mechanistic microbiome research. Nat Med. 2019;25:1442–1452. doi:10.1038/s41591-019-0559-3.
  • Cowardin CA, Ahern PP, Kung VL, Hibberd MC, Cheng J, Guruge JL, Sundaresan V, Head RD, Barile D, Mills DA, et al. Mechanisms by which sialylated milk oligosaccharides impact bone biology in a gnotobiotic mouse model of infant undernutrition. Proc Natl Acad Sci. 2019;116:11988–11996. doi:10.1073/pnas.1821770116.
  • Raman AS, Gehrig JL, Venkatesh S, Chang H-W, Hibberd MC, Subramanian S, Kang G, Bessong PO, Lima AAM, Kosek MN, et al. A sparse covarying unit that describes healthy and impaired human gut microbiota development. Science. 2019;365:eaau4735. doi:10.1126/science.aau4735.
  • Gehrig JL, Venkatesh S, Chang H-W, Hibberd MC, Kung VL, Cheng J, Chen RY, Subramanian S, Cowardin CA, Meier MF, et al. Effects of microbiota-directed foods in gnotobiotic animals and undernourished children. Science. 2019;365:eaau4732. doi:10.1126/science.aau4732.
  • Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257. doi:10.1186/s13059-019-1891-0.
  • Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: estimating species abundance in metagenomics data. PeerJ Comput Sci. 2017;3:e104. doi:10.7717/peerj-cs.104.
  • Pasolli E, Asnicar F, Manara S, Zolfo M, Karcher N, Armanini F, Beghini F, Manghi P, Tett A, Ghensi P, et al. Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell. 2019;176:649–662.e20. doi:10.1016/j.cell.2019.01.001.
  • Nayfach S, Shi ZJ, Seshadri R, Pollard KS, Kyrpides NC. New insights from uncultivated genomes of the global human gut microbiome. Nature. 2019;568:505–510. doi:10.1038/s41586-019-1058-x.
  • Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, Fookes M, Falush D, Keane JA, Parkhill J. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:3691–3693. doi:10.1093/bioinformatics/btv421.
  • Ojima MN, Asao Y, Nakajima A, Katoh T, Kitaoka M, Gotoh A, Hirose J, Urashima T, Fukiya S, Yokota A, et al. Diversification of a fucosyllactose transporter within the genus Bifidobacterium. Appl Environ Microbiol. 2021;88: AEM.01437-21. doi:10.1128/AEM.01437-21.
  • Leth ML, Ejby M, Workman C, Ewald DA, Pedersen SS, Sternberg C, Bahl MI, Licht TR, Aachmann FL, Westereng B, et al. Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut. Nat Microbiol. 2018;3:570–580. doi:10.1038/s41564-018-0132-8.
  • Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Baslé A, Morland C, Day AM, Zheng H, et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat Commun. 2015;6:7481. doi:10.1038/ncomms8481.
  • Lagaert S, Pollet A, Delcour JA, Lavigne R, Courtin CM, Volckaert G. Substrate specificity of three recombinant α-l-arabinofuranosidases from Bifidobacterium adolescentis and their divergent action on arabinoxylan and arabinoxylan oligosaccharides. Biochem Biophys Res Commun. 2010;402:644–650. doi:10.1016/j.bbrc.2010.10.075.
  • Lagaert S, Pollet A, Delcour JA, Lavigne R, Courtin CM, Volckaert G. Characterization of two β-xylosidases from Bifidobacterium adolescentis and their contribution to the hydrolysis of prebiotic xylooligosaccharides. Appl Microbiol Biotechnol. 2011;92:1179–1185. doi:10.1007/s00253-011-3396-y.
  • Rivière A, Moens F, Selak M, Maes D, Weckx S, De Vuyst L. The ability of bifidobacteria to degrade arabinoxylan oligosaccharide constituents and derived oligosaccharides is strain dependent. Appl Environ Microbiol. 2014;80:204–217. doi:10.1128/AEM.02853-13.
  • Vatanen T, Ang QY, Siegwald L, Sarker SA, Le Roy CI, Duboux S, Delannoy-Bruno O, Ngom-Bru C, Boulangé CL, Stražar M, et al. A distinct clade of Bifidobacterium longum in the gut of Bangladeshi children thrives during weaning. Cell. 2022;185:4280–4297.e12. doi:10.1016/j.cell.2022.10.011.
  • Wick RR, Judd LM, Gorrie CL, KE H, Phillippy AM. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol. 2017;13:e1005595. doi:10.1371/journal.pcbi.1005595.
  • Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2015;31:587–589. doi:10.1093/bioinformatics/btu661.
  • Darling ACE, Mau B, Blattner FR, NT P. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394–1403. doi:10.1101/gr.2289704.
  • Darling AE, Mau B, Perna NT, Stajich JE. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5:e11147. doi:10.1371/journal.pone.0011147.
  • Pritchard LH, Glover R, Humphris SG, Elphinstone JK, Toth I. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods. 2016;8:12–24. doi:10.1039/C5AY02550H.
  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069. doi:10.1093/bioinformatics/btu153.
  • Price MN, Dehal PS, Arkin AP, Poon AFY. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5:e9490. doi:10.1371/journal.pone.0009490.
  • Gilchrist CLM, Chooi Y-H, Robinson P. Clinker & clustermap.Js: automatic generation of gene cluster comparison figures. Bioinformatics. 2021;37:2473–2475. doi:10.1093/bioinformatics/btab007.
  • Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014;15:R46. doi:10.1186/gb-2014-15-3-r46.
  • Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B, Terrapon N. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. 2022;50:D571–7. doi:10.1093/nar/gkab1045.
  • 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.
  • Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–101. doi:10.1093/nar/gky418.
  • Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: kEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–731. doi:10.1016/j.jmb.2015.11.006.
  • Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42:D199–205. doi:10.1093/nar/gkt1076.