skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

This content will become publicly available on May 25, 2021

Title: Structural insights into β-1,3-glucan cleavage by a glycoside hydrolase family

Abstract

The fundamental and assorted roles of β-1,3-glucans in nature are underpinned on diverse chemistry and molecular structures, demanding sophisticated and intricate enzymatic systems for their processing. Herein, the selectivity and modes of action of a glycoside hydrolase family active on β-1,3-glucans were systematically investigated combining sequence similarity network, phylogeny, X-ray crystallography, enzyme kinetics, mutagenesis and molecular dynamics. This family exhibits a minimalist and versatile (α/β)-barrel scaffold, which can harbor distinguishing exo or endo modes of action, including an ancillary-binding site for the anchoring of triple-helical β-1,3-glucans. The substrate binding occurs via a hydrophobic knuckle complementary to the canonical curved conformation of β-1,3-glucans or through a substrate conformational change imposed by the active-site topology of some fungal enzymes. Together, these findings expand our understanding of the enzymatic arsenal of bacteria and fungi for the breakdown and modification of β-1,3-glucans, which can be exploited for biotechnological applications.

Authors:
ORCiD logo [1];  [2]; ORCiD logo [1];  [3];  [1];  [1];  [1]; ORCiD logo [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [3]; ORCiD logo [1];  [3]; ORCiD logo [1]
  1. Brazilian Center for Research in Energy and Materials, Campinas, São Paulo (Brazil)
  2. Brazilian Center for Research in Energy and Materials, Campinas, São Paulo (Brazil); Univ. of Campinas (UNICAMP), São Paulo (Brazil)
  3. Univ. of Campinas (UNICAMP), São Paulo (Brazil)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)
OSTI Identifier:
1633140
Grant/Contract Number:  
AC05-00OR22725; AC02-76SF00515; 2015/26982-0; 2013/08293-7; 306135/2016-7
Resource Type:
Accepted Manuscript
Journal Name:
Nature Chemical Biology
Additional Journal Information:
Journal Volume: 16; Journal Issue: 8; Journal ID: ISSN 1552-4450
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; Carbohydrates; Glycobiology; X-ray crystallography

Citation Formats

Santos, Camila R., Costa, Pedro A. C. R., Vieira, Plínio S., Gonzalez, Sinkler E. T., Correa, Thamy L. R., Lima, Evandro A., Mandelli, Fernanda, Pirolla, Renan A. S., Domingues, Mariane N., Cabral, Lucelia, Martins, Marcele P., Cordeiro, Rosa L., Junior, Atílio T., Souza, Beatriz P., Prates, Érica T., Gozzo, Fabio C., Persinoti, Gabriela F., Skaf, Munir S., and Murakami, Mario T. Structural insights into β-1,3-glucan cleavage by a glycoside hydrolase family. United States: N. p., 2020. Web. doi:10.1038/s41589-020-0554-5.
Santos, Camila R., Costa, Pedro A. C. R., Vieira, Plínio S., Gonzalez, Sinkler E. T., Correa, Thamy L. R., Lima, Evandro A., Mandelli, Fernanda, Pirolla, Renan A. S., Domingues, Mariane N., Cabral, Lucelia, Martins, Marcele P., Cordeiro, Rosa L., Junior, Atílio T., Souza, Beatriz P., Prates, Érica T., Gozzo, Fabio C., Persinoti, Gabriela F., Skaf, Munir S., & Murakami, Mario T. Structural insights into β-1,3-glucan cleavage by a glycoside hydrolase family. United States. doi:https://doi.org/10.1038/s41589-020-0554-5
Santos, Camila R., Costa, Pedro A. C. R., Vieira, Plínio S., Gonzalez, Sinkler E. T., Correa, Thamy L. R., Lima, Evandro A., Mandelli, Fernanda, Pirolla, Renan A. S., Domingues, Mariane N., Cabral, Lucelia, Martins, Marcele P., Cordeiro, Rosa L., Junior, Atílio T., Souza, Beatriz P., Prates, Érica T., Gozzo, Fabio C., Persinoti, Gabriela F., Skaf, Munir S., and Murakami, Mario T. Mon . "Structural insights into β-1,3-glucan cleavage by a glycoside hydrolase family". United States. doi:https://doi.org/10.1038/s41589-020-0554-5.
@article{osti_1633140,
title = {Structural insights into β-1,3-glucan cleavage by a glycoside hydrolase family},
author = {Santos, Camila R. and Costa, Pedro A. C. R. and Vieira, Plínio S. and Gonzalez, Sinkler E. T. and Correa, Thamy L. R. and Lima, Evandro A. and Mandelli, Fernanda and Pirolla, Renan A. S. and Domingues, Mariane N. and Cabral, Lucelia and Martins, Marcele P. and Cordeiro, Rosa L. and Junior, Atílio T. and Souza, Beatriz P. and Prates, Érica T. and Gozzo, Fabio C. and Persinoti, Gabriela F. and Skaf, Munir S. and Murakami, Mario T.},
abstractNote = {The fundamental and assorted roles of β-1,3-glucans in nature are underpinned on diverse chemistry and molecular structures, demanding sophisticated and intricate enzymatic systems for their processing. Herein, the selectivity and modes of action of a glycoside hydrolase family active on β-1,3-glucans were systematically investigated combining sequence similarity network, phylogeny, X-ray crystallography, enzyme kinetics, mutagenesis and molecular dynamics. This family exhibits a minimalist and versatile (α/β)-barrel scaffold, which can harbor distinguishing exo or endo modes of action, including an ancillary-binding site for the anchoring of triple-helical β-1,3-glucans. The substrate binding occurs via a hydrophobic knuckle complementary to the canonical curved conformation of β-1,3-glucans or through a substrate conformational change imposed by the active-site topology of some fungal enzymes. Together, these findings expand our understanding of the enzymatic arsenal of bacteria and fungi for the breakdown and modification of β-1,3-glucans, which can be exploited for biotechnological applications.},
doi = {10.1038/s41589-020-0554-5},
journal = {Nature Chemical Biology},
number = 8,
volume = 16,
place = {United States},
year = {2020},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
This content will become publicly available on May 25, 2021
Publisher's Version of Record

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Constant-pressure equations of motion
journal, September 1986


Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks
journal, August 2015

  • Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8
  • DOI: 10.1016/j.bbapap.2015.04.015

Curdlan and other bacterial (1→3)-β-d-glucans
journal, April 2005

  • McIntosh, M.; Stone, B. A.; Stanisich, V. A.
  • Applied Microbiology and Biotechnology, Vol. 68, Issue 2
  • DOI: 10.1007/s00253-005-1959-5

Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997

  • Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
  • DOI: 10.1107/S0907444996012255

Induction of TNF-α production from human peripheral blood monocytes with β-1,3-glucan oligomer prepared from laminarin with β-1,3-glucanase from Bacillus clausii NM-1
journal, January 2003

  • Miyanishi, Nobumitsu; Iwamoto, Yoshiko; Watanabe, Etsuo
  • Journal of Bioscience and Bioengineering, Vol. 95, Issue 2
  • DOI: 10.1016/S1389-1723(03)80128-7

XIP-I, a xylanase inhibitor protein from wheat: a novel protein function
journal, February 2004

  • Juge, Nathalie; Payan, Francoise; Williamson, Gary
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1696, Issue 2
  • DOI: 10.1016/j.bbapap.2003.08.014

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Active Site and Laminarin Binding in Glycoside Hydrolase Family 55
journal, March 2015

  • Bianchetti, Christopher M.; Takasuka, Taichi E.; Deutsch, Sam
  • Journal of Biological Chemistry, Vol. 290, Issue 19
  • DOI: 10.1074/jbc.M114.623579

ATSAS 2.8 : a comprehensive data analysis suite for small-angle scattering from macromolecular solutions
journal, June 2017

  • Franke, D.; Petoukhov, M. V.; Konarev, P. V.
  • Journal of Applied Crystallography, Vol. 50, Issue 4
  • DOI: 10.1107/S1600576717007786

Characterization and Three-dimensional Structures of Two Distinct Bacterial Xyloglucanases from Families GH5 and GH12
journal, March 2007

  • Gloster, Tracey M.; Ibatullin, Farid M.; Macauley, Katherine
  • Journal of Biological Chemistry, Vol. 282, Issue 26
  • DOI: 10.1074/jbc.M700224200

Molecular and Biochemical Characterization of an Endo-β-1,3-glucanase of the Hyperthermophilic Archaeon Pyrococcus furiosus
journal, December 1997

  • Gueguen, Yannick; Voorhorst, Wilfried G. B.; van der Oost, John
  • Journal of Biological Chemistry, Vol. 272, Issue 50
  • DOI: 10.1074/jbc.272.50.31258

Properties of aqueous solutions of lentinan in the absence and presence of zwitterionic surfactants
journal, October 2013


Comparison of simple potential functions for simulating liquid water
journal, July 1983

  • Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
  • The Journal of Chemical Physics, Vol. 79, Issue 2
  • DOI: 10.1063/1.445869

PHENIX : building new software for automated crystallographic structure determination
journal, October 2002

  • Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei
  • Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11
  • DOI: 10.1107/S0907444902016657

Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases.
journal, July 1995

  • Henrissat, B.; Callebaut, I.; Fabrega, S.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 15
  • DOI: 10.1073/pnas.92.15.7090

β-1,3-Glucan Binding by a Thermostable Carbohydrate-Binding Module from Thermotoga maritima
journal, December 2001

  • Boraston, Alisdair B.; Warren, R. Antony J.; Kilburn, Douglas G.
  • Biochemistry, Vol. 40, Issue 48
  • DOI: 10.1021/bi015760g

CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


Constant pressure molecular dynamics simulation: The Langevin piston method
journal, September 1995

  • Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W.
  • The Journal of Chemical Physics, Vol. 103, Issue 11
  • DOI: 10.1063/1.470648

Structure of the gene encoding laminaripentaose-producing β-1,3-glucanase (LPHase) of Streptomyces matensis DIC-108
journal, January 1998

  • Nakabayashi, Masahiro; Nishijima, Takashi; Ehara, Gaku
  • Journal of Fermentation and Bioengineering, Vol. 85, Issue 5
  • DOI: 10.1016/S0922-338X(98)80062-7

XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

Crystal Structure of Glycoside Hydrolase Family 55 β-1,3-Glucanase from the Basidiomycete Phanerochaete chrysosporium
journal, February 2009

  • Ishida, Takuya; Fushinobu, Shinya; Kawai, Rie
  • Journal of Biological Chemistry, Vol. 284, Issue 15
  • DOI: 10.1074/jbc.M808122200

Stereochemistry and the Mechanism of Enzymatic Reactions
journal, November 1953


PULDB: the expanded database of Polysaccharide Utilization Loci
journal, October 2017

  • Terrapon, Nicolas; Lombard, Vincent; Drula, Élodie
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx1022

Unraveling the multivalent binding of a marine family 6 carbohydrate-binding module with its native laminarin ligand
journal, March 2016

  • Jam, Murielle; Ficko-Blean, Elizabeth; Labourel, Aurore
  • The FEBS Journal, Vol. 283, Issue 10
  • DOI: 10.1111/febs.13707

Isolation and characterization of two types of β-1,3-glucanases from the common sea hare Aplysia kurodai
journal, February 2010

  • Kumagai, Yuya; Ojima, Takao
  • Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 155, Issue 2
  • DOI: 10.1016/j.cbpb.2009.10.013

A subfamily roadmap of the evolutionarily diverse glycoside hydrolase family 16 (GH16)
journal, September 2019

  • Viborg, Alexander Holm; Terrapon, Nicolas; Lombard, Vincent
  • Journal of Biological Chemistry, Vol. 294, Issue 44
  • DOI: 10.1074/jbc.RA119.010619

Structure, Mechanistic Action, and Essential Residues of a GH-64 Enzyme, Laminaripentaose-producing β-1,3-Glucanase
journal, July 2009

  • Wu, Hsin-Mao; Liu, Sheng-Wen; Hsu, Ming-Tsung
  • Journal of Biological Chemistry, Vol. 284, Issue 39
  • DOI: 10.1074/jbc.M109.010983

Novel approach to phasing proteins: derivatization by short cryo-soaking with halides
journal, February 2000

  • Dauter, Zbigniew; Dauter, Miroslawa; Rajashankar, K. R.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 2
  • DOI: 10.1107/S0907444999016352

The recognition mechanism of triple-helical β-1,3-glucan by a β-1,3-glucanase
journal, January 2017

  • Qin, Zhen; Yang, Dong; You, Xin
  • Chemical Communications, Vol. 53, Issue 67
  • DOI: 10.1039/C7CC03330C

Functional analysis of hyperthermophilic endocellulase from Pyrococcus horikoshii by crystallographic snapshots
journal, June 2011

  • Kim, Han-Woo; Ishikawa, Kazuhiko
  • Biochemical Journal, Vol. 437, Issue 2
  • DOI: 10.1042/BJ20110292

Privateer: software for the conformational validation of carbohydrate structures
journal, November 2015

  • Agirre, Jon; Iglesias-Fernández, Javier; Rovira, Carme
  • Nature Structural & Molecular Biology, Vol. 22, Issue 11
  • DOI: 10.1038/nsmb.3115

A short history of SHELX
journal, December 2007

  • Sheldrick, George M.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122
  • DOI: 10.1107/S0108767307043930

The structure of a glycoside hydrolase family 81 endo-β-1,3-glucanase
journal, September 2013

  • Zhou, Peng; Chen, Zhongzhou; Yan, Qiaojuan
  • Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 10
  • DOI: 10.1107/S090744491301799X

Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993

  • Darden, Tom; York, Darrin; Pedersen, Lee
  • The Journal of Chemical Physics, Vol. 98, Issue 12
  • DOI: 10.1063/1.464397

Structures and mechanisms of glycosyl hydrolases
journal, September 1995


Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959


The mechanism by which a distinguishing arabinofuranosidase can cope with internal di-substitutions in arabinoxylans
journal, August 2018

  • dos Santos, Camila Ramos; de Giuseppe, Priscila Oliveira; de Souza, Flávio Henrique Moreira
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1212-y

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

Crystal structure and biological implications of a glycoside hydrolase family 55 β-1,3-glucanase from Chaetomium thermophilum
journal, August 2017

  • Papageorgiou, Anastassios C.; Chen, Jinyin; Li, Duochuan
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1865, Issue 8
  • DOI: 10.1016/j.bbapap.2017.05.002

Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA
journal, December 2013


Structural Analysis of a Family 81 Glycoside Hydrolase Implicates Its Recognition of β-1,3-Glucan Quaternary Structure
journal, September 2017


Discovery of novel carbohydrate-active enzymes through the rational exploration of the protein sequences space
journal, March 2019

  • Helbert, William; Poulet, Laurent; Drouillard, Sophie
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 13
  • DOI: 10.1073/pnas.1815791116

Endo-β-1,3-Glucanase GLU1, from the Fruiting Body of Lentinula edodes, Belongs to a New Glycoside Hydrolase Family
journal, September 2011

  • Sakamoto, Yuichi; Nakade, Keiko; Konno, Naotake
  • Applied and Environmental Microbiology, Vol. 77, Issue 23
  • DOI: 10.1128/AEM.05581-11

PACKMOL: A package for building initial configurations for molecular dynamics simulations
journal, October 2009

  • Martínez, L.; Andrade, R.; Birgin, E. G.
  • Journal of Computational Chemistry, Vol. 30, Issue 13
  • DOI: 10.1002/jcc.21224

CHARMM36 United Atom Chain Model for Lipids and Surfactants
journal, January 2014

  • Lee, Sarah; Tran, Alan; Allsopp, Matthew
  • The Journal of Physical Chemistry B, Vol. 118, Issue 2
  • DOI: 10.1021/jp410344g

HMMER web server: interactive sequence similarity searching
journal, May 2011

  • Finn, R. D.; Clements, J.; Eddy, S. R.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr367

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Glucan-like synthetic oligosaccharides: iterative synthesis of linear oligo-β-(1,3)-glucans and immunostimulatory effects
journal, December 2004

  • Jamois, Frank; Ferrières, Vincent; Guégan, Jean-Paul
  • Glycobiology, Vol. 15, Issue 4
  • DOI: 10.1093/glycob/cwi020

FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009

  • Price, M. N.; Dehal, P. S.; Arkin, A. P.
  • Molecular Biology and Evolution, Vol. 26, Issue 7
  • DOI: 10.1093/molbev/msp077

H++ 3.0: automating pK prediction and the preparation of biomolecular structures for atomistic molecular modeling and simulations
journal, May 2012

  • Anandakrishnan, R.; Aguilar, B.; Onufriev, A. V.
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks375

Family 6 Carbohydrate Binding Modules Recognize the Non-reducing End of β-1,3-Linked Glucans by Presenting a Unique Ligand Binding Surface
journal, October 2004

  • van Bueren, Alicia Lammerts; Morland, Carl; Gilbert, Harry J.
  • Journal of Biological Chemistry, Vol. 280, Issue 1
  • DOI: 10.1074/jbc.M410113200

Bacterial 1,3-1,4-β-glucanases: structure, function and protein engineering
journal, December 2000

  • Planas, Antoni
  • Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1543, Issue 2
  • DOI: 10.1016/S0167-4838(00)00231-4

Phaser crystallographic software
journal, July 2007

  • McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
  • Journal of Applied Crystallography, Vol. 40, Issue 4
  • DOI: 10.1107/S0021889807021206