Insights into the dual cleavage activity of the GH16 laminarinase enzyme class on β-1,3 and β-1,4 glycosidic bonds

Liberato, Marcelo Vizona; Prates, Erica Teixeira; Gonçalves, Thiago Augusto; Bernardes, Amanda; Vilela, Nathalia; Fattori, Juliana; Ematsu, Gabriela Cristina; Chinaglia, Mariana; Machi Gomes, Emerson Rodrigo; Migliorini Figueira, Ana Carolina; Damasio, André; Polikarpov, Igor; Skaf, Munir S.; Squina, Fabio Marcio

doi:10.1016/j.jbc.2021.100385

Title: Insights into the dual cleavage activity of the GH16 laminarinase enzyme class on β-1,3 and β-1,4 glycosidic bonds

Journal Article · Mon Feb 01 00:00:00 EST 2021 · Journal of Biological Chemistry

DOI:https://doi.org/10.1016/j.jbc.2021.100385· OSTI ID:1767876

Liberato, Marcelo Vizona ^[1]; Prates, Erica Teixeira ^[2]; Gonçalves, Thiago Augusto ^[3]; Bernardes, Amanda ^[4]; Vilela, Nathalia ^[3]; Fattori, Juliana ^[5]; Ematsu, Gabriela Cristina ^[6]; Chinaglia, Mariana ^[6]; Machi Gomes, Emerson Rodrigo ^[6]; Migliorini Figueira, Ana Carolina ^[5]; Damasio, André ^[7]; Polikarpov, Igor ^[8]; Skaf, Munir S. ^[9]; Squina, Fabio Marcio ^[10]

Lab. Nacional de Ciencia e Tecnologia do Bioetanol (CTBE), Campinas (Brazil); Univ. de Sorocaba (Brazil)
Univ. of Campinas (UNICAMP), Sao Paulo (Brazil); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. de Sorocaba (Brazil); Univ. of Campinas (Brazil)
Univ. de Sao Paolo (Brazil)
Lab. Nacional de Biociencias (LNBio), Campinas (Brazil)
Lab. Nacional de Ciencia e Tecnologia do Bioetanol (CTBE), Campinas (Brazil)
Univ. of Campinas (Brazil)
Univ. of Sao Paulo (Brazil)
Univ. of Campinas (UNICAMP), Sao Paulo (Brazil)
Univ. de Sorocaba (Brazil)

Glycoside hydrolases (GH) are involved in the degradation of a wide diversity of carbohydrates and present several biotechnological applications. Many GH families are composed of enzymes with a single well-defined specificity. In contrast, enzymes from the GH16 family can act on a range of different polysaccharides, including β-glucans and galactans. SCLam, a GH16 member derived from a soil metagenome, an endo-β-1,3(4)-glucanase (EC 3.2.1.6), can cleave both β-1,3 and β-1,4 glycosidic bonds in glucans, such as laminarin, barley β-glucan, and cello-oligosaccharides. A similar cleavage pattern was previously reported for other GH16 family members. However, the molecular mechanisms for this dual cleavage activity on (1,3)- and (1,4)-β-D-glycosidic bonds by laminarinases have not been elucidated. In this sense, we determined the X-ray structure of a presumably inactive form of SCLam co-crystallized with different oligosaccharides. The solved structures revealed general bound products that are formed due to residual activities of hydrolysis and transglycosylation. Biochemical and biophysical analyses and molecular dynamics simulations help to rationalize differences in activity towards different substrates. Our results depicted a bulky aromatic residue near the catalytic site critical to select the preferable configuration of glycosidic bonds in the binding cleft. Altogether, these data contribute to understanding the structural basis of recognition and hydrolysis of β-1,3 and β-1,4 glycosidic linkages of the laminarinase enzyme class, which is valuable for future studies on the GH16 family members and applications related to biomass conversion into feedstocks and bioproducts.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); FAPESP

Grant/Contract Number:: AC05-00OR22725; 2015/50590-4; 2013/15582-5

OSTI ID:: 1767876

Journal Information:: Journal of Biological Chemistry, Vol. 296; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
glycoside hydrolase
transglycosylation
GH16
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endo-1
3(4)-beta-glucanases
metagenome

Title: Insights into the dual cleavage activity of the GH16 laminarinase enzyme class on β-1,3 and β-1,4 glycosidic bonds

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