Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis

Mikiyasu Sakanaka, Morten Ejby Hansen, Aina Gotoh, Toshihiko Katoh, Keisuke Yoshida, Toshitaka Odamaki, Hiroyuki Yachi, Yuta Sugiyama, Shin Kurihara, Junko Hirose, Tadasu Urashima, Jin zhong Xiao, Motomitsu Kitaoka, Satoru Fukiya, Atsushi Yokota, Leila Lo Leggio, Maher Abou Hachem*, Takane Katayama

*Corresponding author for this work

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Abstract

The human gut microbiota established during infancy has persistent effects on health. In vitro studies have suggested that human milk oligosaccharides (HMOs) in breast milk promote the formation of a bifidobacteria-rich microbiota in infant guts; however, the underlying molecular mechanism remains elusive. Here, we characterized two functionally distinct but overlapping fucosyllactose transporters (FL transporter-1 and -2) from Bifidobacterium longum subspecies infantis. Fecal DNA and HMO consumption analyses, combined with deposited metagenome data mining, revealed that FL transporter-2 is primarily associated with the bifidobacteria-rich microbiota formation in breast-fed infant guts. Structural analyses of the solute-binding protein (SBP) of FL transporter-2 complexed with 2′-fucosyllactose and 3-fucosyllactose, together with phylogenetic analysis of SBP homologs of both FL transporters, highlight a unique adaptation strategy of Bifidobacterium to HMOs, in which the gain-of-function mutations enable FL transporter-2 to efficiently capture major fucosylated HMOs. Our results provide a molecular insight into HMO-mediated symbiosis and coevolution between bifidobacteria and humans.
Original languageEnglish
Article numbereaaw7696
JournalScience Advances
Volume5
Issue number8
Number of pages16
ISSN2375-2548
DOIs
Publication statusPublished - 2019

Cite this

Sakanaka, M., Hansen, M. E., Gotoh, A., Katoh, T., Yoshida, K., Odamaki, T., ... Katayama, T. (2019). Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. Science Advances, 5(8), [eaaw7696]. https://doi.org/10.1126/sciadv.aaw7696
Sakanaka, Mikiyasu ; Hansen, Morten Ejby ; Gotoh, Aina ; Katoh, Toshihiko ; Yoshida, Keisuke ; Odamaki, Toshitaka ; Yachi, Hiroyuki ; Sugiyama, Yuta ; Kurihara, Shin ; Hirose, Junko ; Urashima, Tadasu ; Xiao, Jin zhong ; Kitaoka, Motomitsu ; Fukiya, Satoru ; Yokota, Atsushi ; Leggio, Leila Lo ; Abou Hachem, Maher ; Katayama, Takane. / Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. In: Science Advances. 2019 ; Vol. 5, No. 8.
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title = "Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis",
abstract = "The human gut microbiota established during infancy has persistent effects on health. In vitro studies have suggested that human milk oligosaccharides (HMOs) in breast milk promote the formation of a bifidobacteria-rich microbiota in infant guts; however, the underlying molecular mechanism remains elusive. Here, we characterized two functionally distinct but overlapping fucosyllactose transporters (FL transporter-1 and -2) from Bifidobacterium longum subspecies infantis. Fecal DNA and HMO consumption analyses, combined with deposited metagenome data mining, revealed that FL transporter-2 is primarily associated with the bifidobacteria-rich microbiota formation in breast-fed infant guts. Structural analyses of the solute-binding protein (SBP) of FL transporter-2 complexed with 2′-fucosyllactose and 3-fucosyllactose, together with phylogenetic analysis of SBP homologs of both FL transporters, highlight a unique adaptation strategy of Bifidobacterium to HMOs, in which the gain-of-function mutations enable FL transporter-2 to efficiently capture major fucosylated HMOs. Our results provide a molecular insight into HMO-mediated symbiosis and coevolution between bifidobacteria and humans.",
author = "Mikiyasu Sakanaka and Hansen, {Morten Ejby} and Aina Gotoh and Toshihiko Katoh and Keisuke Yoshida and Toshitaka Odamaki and Hiroyuki Yachi and Yuta Sugiyama and Shin Kurihara and Junko Hirose and Tadasu Urashima and Xiao, {Jin zhong} and Motomitsu Kitaoka and Satoru Fukiya and Atsushi Yokota and Leggio, {Leila Lo} and {Abou Hachem}, Maher and Takane Katayama",
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doi = "10.1126/sciadv.aaw7696",
language = "English",
volume = "5",
journal = "Science Advances",
issn = "2375-2548",
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Sakanaka, M, Hansen, ME, Gotoh, A, Katoh, T, Yoshida, K, Odamaki, T, Yachi, H, Sugiyama, Y, Kurihara, S, Hirose, J, Urashima, T, Xiao, JZ, Kitaoka, M, Fukiya, S, Yokota, A, Leggio, LL, Abou Hachem, M & Katayama, T 2019, 'Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis', Science Advances, vol. 5, no. 8, eaaw7696. https://doi.org/10.1126/sciadv.aaw7696

Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. / Sakanaka, Mikiyasu; Hansen, Morten Ejby; Gotoh, Aina; Katoh, Toshihiko; Yoshida, Keisuke; Odamaki, Toshitaka; Yachi, Hiroyuki; Sugiyama, Yuta; Kurihara, Shin; Hirose, Junko; Urashima, Tadasu; Xiao, Jin zhong; Kitaoka, Motomitsu; Fukiya, Satoru; Yokota, Atsushi; Leggio, Leila Lo; Abou Hachem, Maher ; Katayama, Takane.

In: Science Advances, Vol. 5, No. 8, eaaw7696, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis

AU - Sakanaka, Mikiyasu

AU - Hansen, Morten Ejby

AU - Gotoh, Aina

AU - Katoh, Toshihiko

AU - Yoshida, Keisuke

AU - Odamaki, Toshitaka

AU - Yachi, Hiroyuki

AU - Sugiyama, Yuta

AU - Kurihara, Shin

AU - Hirose, Junko

AU - Urashima, Tadasu

AU - Xiao, Jin zhong

AU - Kitaoka, Motomitsu

AU - Fukiya, Satoru

AU - Yokota, Atsushi

AU - Leggio, Leila Lo

AU - Abou Hachem, Maher

AU - Katayama, Takane

PY - 2019

Y1 - 2019

N2 - The human gut microbiota established during infancy has persistent effects on health. In vitro studies have suggested that human milk oligosaccharides (HMOs) in breast milk promote the formation of a bifidobacteria-rich microbiota in infant guts; however, the underlying molecular mechanism remains elusive. Here, we characterized two functionally distinct but overlapping fucosyllactose transporters (FL transporter-1 and -2) from Bifidobacterium longum subspecies infantis. Fecal DNA and HMO consumption analyses, combined with deposited metagenome data mining, revealed that FL transporter-2 is primarily associated with the bifidobacteria-rich microbiota formation in breast-fed infant guts. Structural analyses of the solute-binding protein (SBP) of FL transporter-2 complexed with 2′-fucosyllactose and 3-fucosyllactose, together with phylogenetic analysis of SBP homologs of both FL transporters, highlight a unique adaptation strategy of Bifidobacterium to HMOs, in which the gain-of-function mutations enable FL transporter-2 to efficiently capture major fucosylated HMOs. Our results provide a molecular insight into HMO-mediated symbiosis and coevolution between bifidobacteria and humans.

AB - The human gut microbiota established during infancy has persistent effects on health. In vitro studies have suggested that human milk oligosaccharides (HMOs) in breast milk promote the formation of a bifidobacteria-rich microbiota in infant guts; however, the underlying molecular mechanism remains elusive. Here, we characterized two functionally distinct but overlapping fucosyllactose transporters (FL transporter-1 and -2) from Bifidobacterium longum subspecies infantis. Fecal DNA and HMO consumption analyses, combined with deposited metagenome data mining, revealed that FL transporter-2 is primarily associated with the bifidobacteria-rich microbiota formation in breast-fed infant guts. Structural analyses of the solute-binding protein (SBP) of FL transporter-2 complexed with 2′-fucosyllactose and 3-fucosyllactose, together with phylogenetic analysis of SBP homologs of both FL transporters, highlight a unique adaptation strategy of Bifidobacterium to HMOs, in which the gain-of-function mutations enable FL transporter-2 to efficiently capture major fucosylated HMOs. Our results provide a molecular insight into HMO-mediated symbiosis and coevolution between bifidobacteria and humans.

U2 - 10.1126/sciadv.aaw7696

DO - 10.1126/sciadv.aaw7696

M3 - Journal article

VL - 5

JO - Science Advances

JF - Science Advances

SN - 2375-2548

IS - 8

M1 - eaaw7696

ER -