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Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides

Ojima, Miriam N. Jiang, Lin Arzamasov, Aleksandr A. Yoshida, Keisuke Odamaki, Toshitaka Xiao, Jinzhong Nakajima, Aruto Kitaoka, Motomitsu Hirose, Junko Urashima, Tadasu Katoh, Toshihiko Gotoh, Aina van Sinderen, Douwe Rodionov, Dmitry A. Osterman, Andrei L. Sakanaka, Mikiyasu Katayama, Takane 京都大学 DOI:10.1038/s41396-022-01270-3

2022.09

概要

Bifidobacteria are among the first colonizers of the infant gut, and human milk oligosaccharides (HMOs) in breastmilk are instrumental for the formation of a bifidobacteria-rich microbiota. However, little is known about the assembly of bifidobacterial communities. Here, by applying assembly theory to a community of four representative infant-gut associated Bifidobacterium species that employ varied strategies for HMO consumption, we show that arrival order and sugar consumption phenotypes significantly affected community formation. Bifidobacterium bifidum and Bifidobacterium longum subsp. infantis, two avid HMO consumers, dominate through inhibitory priority effects. On the other hand, Bifidobacterium breve, a species with limited HMO-utilization ability, can benefit from facilitative priority effects and dominates by utilizing fucose, an HMO degradant not utilized by the other bifidobacterial species. Analysis of publicly available breastfed infant faecal metagenome data showed that the observed trends for B. breve were consistent with our in vitro data, suggesting that priority effects may have contributed to its dominance. Our study highlights the importance and history dependency of initial community assembly and its implications for the maturation trajectory of the infant gut microbiota.

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参考文献

1. Turroni F, Milani C, Duranti S, Lugli GA, Bernasconi S, Margolles A, et al. The infant gut microbiome as a microbial organ influencing host well-being. Ital J Pediatr. 2020;46:1–13.

2. Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8:343ra82–343ra82.

3. Akagawa S, Tsuji S, Onuma C, Akagawa Y, Yamaguchi T, Yamagishi M, et al. Effect of delivery mode and nutrition on gut microbiota in neonates. Ann Nutr Metab. 2019;74:132–9.

4. Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 2018;555:210–5.

5. Vellend M, Srivastava DS, Anderson KM, Brown CD, Jankowski JE, Kleynhans EJ, et al. Assessing the relative importance of neutral stochasticity in ecological communities. Oikos. 2014;123:1420–30.

6. Fukami T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst. 2015;46:1–23.

7. Fukami T, Nakajima M. Community assembly: Alternative stable states or alter- native transient states? Ecol Lett. 2011;14:973–84.

8. Sprockett D, Fukami T, Relman DA. Role of priority effects in the early-life assembly of the gut microbiota. Nat Rev Gastroenterol Hepatol. 2018;15:197–205.

9. Debray R, Herbert RA, Jaffe AL, Crits-Christoph A, Power ME, Koskella B. Priority effects in microbiome assembly. Nat Rev Microbiol. 2022;20:109–21.

10. Tannock GW, Lawley B, Munro K, Pathmanathan SG, Zhou SJ, Makrides M, et al. Comparison of the compositions of the stool microbiotas of infants fed goat milk formula, cow milk-based formula, or breast milk. Appl Environ Microbiol. 2013;79:3040–8.

11. 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.

12. Sakanaka M, Hansen ME, Gotoh A, Katoh T, Yoshida K, Odamaki T, et al. Evolu- tionary adaptation in fucosyllactose uptake systems supports bifidobacteria- infant symbiosis. Sci Adv. 2019;5:eaaw7696.

13. Engfer MB, Stahl B, Finke B, Sawatzki G, Daniel H. Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract. Am J Clin Nutr. 2000;71:1589–96.

14. Macrobal A, Sonnenburg JL. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect. 2012;18:12–15.

15. Macrobal A, Barboza M, Froehlich JW, Block DE, German JB, Lebrilla CB, et al. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem. 2010;58:5334–40.

16. Sakanaka M, Gotoh A, Yoshida K, Odamaki T, Koguchi H, Xiao JZ, et al. Varied pathways of infant gut-associated Bifidobacterium to assimilate human milk oli- gosaccharides: prevalence of the gene set and its correlation with bifidobacteria- rich microbiota formation. Nutrients. 2020;12:71.

17. Katayama T. Host-derived glycans serve as selected nutrients for the gut microbe: human milk oligosaccharides and bifidobacteria. Biosci Biotechnol Biochem. 2016;80:621–32.

18. Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, Merusi P, et al. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol. 2009;75:1534–45.

19. Gore C, Munro K, Lay C, Bibiloni R, Morris J, Woodcock A, et al. Bifidobacterium pseudocatenulatum is associated with atopic eczema: A nested case-control study investigating the fecal microbiota of infants. J Allergy Clin Immunol. 2008;121:135–40.

20. Lewis ZT, Mills DA. Differential establishment of bifidobacteria in the breastfed infant gut. Nestle Nutr Inst Work Ser. 2017;88:149–59.

21. Tannock GW, Lee PS, Wong KH, Lawley B. Why don’t all infants have bifido- bacteria in their stool? Front Microbiol. 2016;7:6–10.

22. Reyman M, van Houten MA, van Baarle D, Bosch AATM, Man WH, Chu MLJN, et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;10:1–12.

23. Underwood MA, Kalanetra KM, Bokulich NA, Lewis ZT, Mirmiran M, Tancredi DJ, et al. A comparison of two probiotic strains of bifidobacteria in preterm infants. J Pediatr. 2013;163:1585–91.

24. Plummer EL, Bulach DM, Murray GL, Jacobs SE, Tabrizi SN, Garland SM. Gut microbiota of preterm infants supplemented with probiotics: sub-study of the ProPrems trial. BMC Microbiol. 2018;18:1–8.

25. Kitajima H, Sumida Y, Tanaka R, Yuki N, Takayama H, Fujimura M. Early admin- istration of Bifidobacterium breve to preterm infants: Randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 1997;76:101–7.

26. Ojima MN, Yoshida K, Sakanaka M, Jiang L, Odamaki T, Katayama T. Ecological and molecular perspectives on responders and non-responders to probiotics and prebiotics. Curr Opin Biotechnol. 2022;73:108–20.

27. Suez J, Zmora N, Segal E, Elinav E. The pros, cons, and many unknowns of probiotics. Nat Med. 2019;25:716–29.

28. Costeloe K, Hardy P, Juszczak E, Wilks M, Millar MR. Bifidobacterium breve BBG-001 in very preterm infants: A randomised controlled phase 3 trial. Lancet. 2016;387:649–60.

29. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 2005;33:5691–702.

30. Katoh T, Ojima MN, Sakanaka M, Ashida H, Gotoh A, Katayama T. Enzymatic adaptation of Bifidobacterium bifidum to host glycans, viewed from glycoside hydrolyases and carbohydrate-binding modules. Microorganisms. 2020;8:481.

31. Egan M, Motherway MO, Kilcoyne M, Kane M, Joshi L, Ventura M, et al. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol. 2014;14:1–14.

32. Higgins MA, Ryan KS. Generating a fucose permease deletion mutant in Bifido- bacterium longum subspecies infantis ATCC 15697. Anaerobe. 2021;68:102320.

33. O’Connell Motherway M, Kinsella M, Fitzgerald GF, van Sinderen D. Transcrip- tional and functional characterization of genetic elements involved in galacto- oligosaccharide utilization by Bifidobacterium breve UCC2003. Micro Biotechnol. 2013;6:67–79.

34. Yoshida E, Sakurama H, Kiyohara M, Nakajima M, Kitaoka M, Ashida H, et al. Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glyco- biology. 2012;22:361–8.

35. Vannette RL, Fukami T. Historical contingency in species interactions: Towards niche-based predictions. Ecol Lett. 2014;17:115–24.

36. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.

37. Pu Z, Jiang L. Dispersal among local communities does not reduce historical contingencies during metacommunity assembly. Oikos. 2015;124:1327–36.

38. Chase JM. Community assembly: when should history matter? Oecologia. 2003;136:489–98.

39. Schröder A, Persson L, De Roos AM. Direct experimental evidence for alternative stable states: A review. Oikos. 2005;110:3–19.

40. Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, et al. Physiology of consumption of human milk oligosaccharides by infant gut- associated bifidobacteria. J Biol Chem. 2011;286:34583–92.

41. Gotoh A, Katoh T, Sakanaka M, Ling Y, Yamada C, Asakuma S, et al. Sharing of human milk oligosaccharides degradants within bifidobacterial communities in faecal cul- tures supplemented with Bifidobacterium bifidum. Sci Rep. 2018;8:13958.

42. Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, Kumagai H, et al. Two distinct α- L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology. 2009;19: 1010–7.

43. Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology. 2010;156:3329–41.

44. Avershina E, Storrø O, Øien T, Johnsen R, Wilson R, Egeland T, et al. Bifidobacterial succession and correlation networks in a large unselected cohort of mothers and their children. Appl Environ Microbiol. 2013;79:497–507.

45. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, et al. Diversity of bifidobacteria within the infant gut microbiota. PLoS One. 2012;7:20–4.

46. James K, Bottacini F, Contreras JIS, Vigoureux M, Egan M, Motherway MO, et al. Metabolism of the predominant human milk oligosaccharide fucosyllactose by an infant gut commensal. Sci Rep. 2019;9:1–20.

47. Dedon LR, Özcan E, Rani A, Sela DA. Bifidobacterium infantis metabolizes 2′ fucosyllactose-derived and free fucose through a common catabolic pathway resulting in 1,2-propanediol secretion. Front Nutr. 2020;7:1–16.

48. Sprockett D, Martin M, Costello E, Burns A, Holmes S, Gurven M, et al. Microbiota assembly, structure, and dynamics among tsimane horticulturalists of the Boli- vian Amazon. Nat Commun. 2019;11:1–14.

49. Laursen MF, Sakanaka M, von Burg N, Mörbe U, Andersen D, Moll JM, et al. Bifidobacterium species associated with breastfeeding produce aromatic lactic acids in the infant gut. Nat Microbiol. 2021;6:1367–82.

50. Meng D, Sommella E, Salviati E, Campiglia P, Ganguli K, Djebali K, et al. Indole-3- lactic acid, a metabolite of tryptophan, secreted by Bifidobacterium longum subspecies infantis is anti-inflammatory in the immature intestine. Pediatr Res. 2020;88:209–17.

51. Bunesova V, Lacroix C, Schwab C. Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense. BMC Microbiol. 2016;16:248.

52. Ruiz-Moyano S, Totten SM, Garrido D, 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.

53. Lawson MAE, O’Neill IJ, Kujawska M, Gowrinadh Javvadi S, Wijeyesekera A, Flegg Z, et al. Breast milk-derived human milk oligosaccharides promote Bifidobacter- ium interactions within a single ecosystem. ISME J. 2020;14:635–48.

54. Schwab C, Ruscheweyh HJ, Bunesova V, Pham VT, Beerenwinkel N, Lacroix C. Trophic interactions of infant bifidobacteria and Eubacterium hallii during L- fucose and fucosyllactose degradation. Front Microbiol. 2017;8:1–14.

55. Engels C, Ruscheweyh HJ, Beerenwinkel N, Lacroix C, Schwab C. The common gut microbe Eubacterium hallii also contributes to intestinal propionate formation. Front Microbiol. 2016;7:1–12.

56. Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC, Desai P, et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe. 2011;10:507–14.

57. Vatanen T, Kostic AD, D’Hennezel E, Siljander H, Franzosa EA, Yassour M, et al. Variation in Microbiome LPS Immunogenicity Contributes to Autoimmunity in Humans. Cell. 2016;165:842–53.

58. Vatanen T, Franzosa EA, Schwager R, Tripathi S, Arthur TD, Vehik K, et al. The human gut microbiome in early-onset type 1 diabetes from the TEDDY study. Nature. 2018;562:589–94.

59. Moossavi S, Sepehri S, Robertson B, Bode L, Goruk S, Field CJ, et al. Composition and Variation of the Human Milk Microbiota Are Influenced by Maternal and Early-Life Factors. Cell Host Microbe. 2019;25:324–335.e4.

60. Martín R, Langa S, Reviriego C, Jiménez E, Marín ML, Xaus J, et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr. 2003;143:754–8.

61. Martín R, Jiménez E, Heilig H, Fernández L, Marín ML, Zoetendal EG, et al. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial popu- lation by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl Environ Microbiol. 2009;75:965–9.

62. Heikkilä MP, Saris PEJ. Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol. 2003;95:471–8.

63. Li Y, Shimizu T, Hosaka A, Kaneko N, Ohtsuka Y, Yamashiro Y. Effects of Bifido- bacterium breve supplementation on intestinal flora of low birth weight infants. Pediatr Int. 2004;46:509–15.

64. Nishimoto M, Kitaoka M. Practical preparation of lacto-N-biose I, a candidate for the bifidus factor in human milk. Biosci Biotechnol Biochem. 2007;71:2101–4.

65. Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52:2141–6.

66. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA, Stares MD, et al. Cul- turing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature. 2016;533:543–6.

67. Tanizawa Y, Fujisawa T, Kaminuma E, Nakamura Y. Arita M. DFAST and DAGA: Web-based integrated genome annotation tools and resources. Biosci Micro- biota, Food Heal. 2016;35:173–84.

68. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014;42:206–14.

69. Price MN, Arkin AP. PaperBLAST: Text-mining papers for information about homologs. bioRxiv. 2017;2:1–10.

70. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:490–5.

71. Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C, Moreno-Hagelsieb G. The Trans- porter Classification Database (TCDB): Recent advances. Nucleic Acids Res. 2016;44:D372–9.

72. Martínez I, Wallace G, Zhang C, Legge R, Benson AK, Carr TP, et al. Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol. 2009;75:4175–84.

73. Anumula KR. Advances in fluorescence derivatization methods for high- performance liquid chromatographic analysis of glycoprotein carbohydrates. Anal Biochem. 2006;350:1–23.

74. Cohenford MA, Abraham A, Abraham J, Dain JA. Colorimetric assay for free and bound L-fucose. Anal Biochem. 1989;177:172–7.

75. Kato K, Odamaki T, Mitsuyama E, Sugahara H, Xiao JZ, Osawa R. Age-related changes in the composition of gut Bifidobacterium species. Curr Microbiol. 2017;74:987–95.

76. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.

77. Martin M. Cutadapt removes adapter sequences from high-throughput sequen- cing reads. EMBnet. 2011;17:10–12.

78. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:1–13.

79. Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: Estimating species abun- dance in metagenomics data. PeerJ Comput Sci. 2017;2017:1–17.

80. Milani C, Lugli GA, Fontana F, Mancabelli L, Alessandri G, Longhi G, et al. METAnnotatorX2: A comprehensive tool for deep and shallow metagenomic data set analyses. mSystems. 2021;6:1–15.

81. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. 2019.

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