Outer membrane utilisomes mediate glycan uptake in gut Bacteroidetes

Joshua B. R. White, Augustinas Silale, Matthew Feasey, Tiaan Heunis, Yiling Zhu, Hong Zheng, Akshada Gajbhiye, Susan Firbank, Arnaud Baslé, Matthias Trost, David N. Bolam, Bert Berg () and Neil A. Ranson ()
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Joshua B. R. White: University of Leeds
Augustinas Silale: Newcastle University
Matthew Feasey: Newcastle University
Tiaan Heunis: Newcastle University
Yiling Zhu: Newcastle University
Hong Zheng: Newcastle University
Akshada Gajbhiye: Newcastle University
Susan Firbank: Newcastle University
Arnaud Baslé: Newcastle University
Matthias Trost: Newcastle University
David N. Bolam: Newcastle University
Bert Berg: Newcastle University
Neil A. Ranson: University of Leeds

Nature, 2023, vol. 618, issue 7965, 583-589

Abstract: Abstract Bacteroidetes are abundant members of the human microbiota, utilizing a myriad of diet- and host-derived glycans in the distal gut1. Glycan uptake across the bacterial outer membrane of these bacteria is mediated by SusCD protein complexes, comprising a membrane-embedded barrel and a lipoprotein lid, which is thought to open and close to facilitate substrate binding and transport. However, surface-exposed glycan-binding proteins and glycoside hydrolases also play critical roles in the capture, processing and transport of large glycan chains. The interactions between these components in the outer membrane are poorly understood, despite being crucial for nutrient acquisition by our colonic microbiota. Here we show that for both the levan and dextran utilization systems of Bacteroides thetaiotaomicron, the additional outer membrane components assemble on the core SusCD transporter, forming stable glycan-utilizing machines that we term utilisomes. Single-particle cryogenic electron microscopy structures in the absence and presence of substrate reveal concerted conformational changes that demonstrate the mechanism of substrate capture, and rationalize the role of each component in the utilisome.

Date: 2023
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DOI: 10.1038/s41586-023-06146-w

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