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

doi:10.1126/sciadv.aaw7696

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

Department of Chemistry

30 Citations (Scopus)

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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 language	English
Article number	eaaw7696
Journal	Science Advances
Volume	5
Issue number	8
Pages (from-to)	1-15
Number of pages	15
ISSN	2375-2548
DOIs	https://doi.org/10.1126/sciadv.aaw7696
Publication status	Published - 28 Aug 2019

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Sakanaka, M., Hansen, M. E., Gotoh, A., Katoh, T., Yoshida, K., Odamaki, T., Yachi, H., Sugiyama, Y., Kurihara, S., Hirose, J., Urashima, T., Xiao, J., Kitaoka, M., Fukiya, S., Yokota, A., Lo Leggio, L., Abou Hachem, M., & Katayama, T. (2019). Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis. Science Advances, 5(8), 1-15. [eaaw7696]. https://doi.org/10.1126/sciadv.aaw7696

Sakanaka, M, Hansen, ME, Gotoh, A, Katoh, T, Yoshida, K, Odamaki, T, Yachi, H, Sugiyama, Y, Kurihara, S, Hirose, J, Urashima, T, Xiao, J, Kitaoka, M, Fukiya, S, Yokota, A, Lo Leggio, L, Abou Hachem, M & Katayama, T 2019, 'Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis', Science Advances, vol. 5, no. 8, eaaw7696, pp. 1-15. https://doi.org/10.1126/sciadv.aaw7696

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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.",

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 Jin-zhong Xiao and Motomitsu Kitaoka and Satoru Fukiya and Atsushi Yokota and {Lo Leggio}, Leila and {Abou Hachem}, Maher and Takane Katayama",

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AU - Sakanaka, Mikiyasu

AU - Hansen, Morten Ejby

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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 - Lo Leggio, Leila

AU - Abou Hachem, Maher

AU - Katayama, Takane

PY - 2019/8/28

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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.

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DO - 10.1126/sciadv.aaw7696

M3 - Journal article

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JO - Science advances

JF - Science advances

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ER -

Evolutionary adaptation in fucosyllactose uptake systems supports bifidobacteria-infant symbiosis

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