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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]
+ Show Author Affiliations
  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.
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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. https://doi.org/10.1038/s41589-020-0554-5
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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. https://doi.org/10.1038/s41589-020-0554-5. https://www.osti.gov/servlets/purl/1633140.
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@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}
}
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