Bacterial polysaccharide lyase family 33: Specificity from an evolutionarily conserved binding tunnel

M Mélanie Loiodice (Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales) E Elodie Drula (Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Univ, CNRS, Institut National de Recherche pour l'Agriculture, l'alimentation et l'Environnement) Z Zak McIver S Svetlana Antonyuk (Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool) A Arnaud Basle M Marcelo Lima (School of Life Sciences, Keele University) E Edwin A. Yates (Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool) D Dominic P. Byrne (Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool) J Jamie Coughlan (Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool) A Andrew Leech (Department of Biology, Technology Facility, University of York) S Shahram Mesdaghi (Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool) D Daniel J. Rigden (Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool) S Sophie Drouillard (Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales) W William Helbert (Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales) B Bernard Henrissat N Nicolas Terrapon G Gareth S. A. Wright (School of Life Sciences, University of Essex) M Marie Couturier (Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales) A Alan Cartmell

Abstract

Acidic glycans are essential for the biology of multicellular eukaryotes. To utilize them, microbial life including symbionts and pathogens has evolved polysaccharide lyases (PL) that cleave their 1,4 glycosidic linkages via a β-elimination mechanism. PL family 33 (PL33) enzymes have the unusual ability to target a diverse range of glycosaminoglycans (GAGs), as well as the bacterial polymer, gellan gum. In order to gain more detailed insight into PL33 activities we recombinantly expressed 10 PL33 members derived from all major environments and further elucidated the detailed biochemical and biophysical properties of five, showing that their substrate specificity is conferred by variations in tunnel length and topography. The key amino acids involved in catalysis and substrate interactions were identified, and employing a combination of complementary biochemical, structural, and modeling approaches, we show that the tunnel topography is induced by substrate binding to the glycan. Structural and bioinformatic analyses revealed that these features are conserved across several lyase families as well as in mammalian GAG epimerases.

Article Details

Volume / Issue Vol. 122, Issue 7
Published February 18, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (19)

M

Mélanie Loiodice

Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales

E

Elodie Drula

Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Univ, CNRS, Institut National de Recherche pour l'Agriculture, l'alimentation et l'Environnement

Z

Zak McIver

S

Svetlana Antonyuk

Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool

A

Arnaud Basle

M

Marcelo Lima

School of Life Sciences, Keele University

E

Edwin A. Yates

Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool

D

Dominic P. Byrne

Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool

J

Jamie Coughlan

Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool

A

Andrew Leech

Department of Biology, Technology Facility, University of York

S

Shahram Mesdaghi

Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool

D

Daniel J. Rigden

Department of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool

S

Sophie Drouillard

Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales

W

William Helbert

Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales

B

Bernard Henrissat

N

Nicolas Terrapon

G

Gareth S. A. Wright

School of Life Sciences, University of Essex

M

Marie Couturier

Université Grenoble Alpes, CNRS, Centre de Recherche sur les Macromolécules Végétales

A

Alan Cartmell