Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases

TY - JOUR

T1 - Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases

AU - Franco Cairo, João Paulo

AU - Mandelli, Fernanda

AU - Tramontina, Robson

AU - Cannella, David

AU - Paradisi, Alessandro

AU - Ciano, Luisa

AU - Ferreira, Marcel

AU - Liberato, Marcelo Vizoná

AU - Brenelli, Lívia

AU - Gonçalves, Thiago

AU - Rodrigues, Gisele Nunes

AU - Alvarez, Thabata Maria

AU - Mofatto, Luciana Souto

AU - Carazzolle, Marcelo Falsarella

AU - Pradella, José Geraldo

AU - Leme, Adriana Paes

AU - Costa-Leonardo, Ana Maria

AU - Oliveira Neto, Mario

AU - Damasio, André

AU - Davies, Gideon

AU - Felby, Claus

AU - Walton, Paul Howard

AU - Squina, Fabio

N1 - © The Royal Society of Chemistry 2022

PY - 2022/6/21

Y1 - 2022/6/21

N2 - Wood-feeding termites effectively degrade plant biomass through enzymatic degradation. Despite their high efficiencies, however, individual glycoside hydrolases isolated from termites and their symbionts exhibit anomalously low effectiveness in lignocellulose degradation, suggesting hereto unknown enzymatic activities in their digestome. Herein, we demonstrate that an ancient redox-active enzyme encoded by the lower termite Coptotermes gestroi, a Cu/Zn superoxide dismutase (CgSOD-1) plays a previously unknown role in plant biomass degradation. We show that CgSOD-1 transcripts and peptides are up-regulated in response to an increased level of lignocellulose recalcitrance and that CgSOD-1 localizes in the lumen of the fore- and midguts of C. gestroi together with termite main cellulase, CgEG-1-GH9. CgSOD-1 boosts the saccharification of polysaccharides by CgEG-1-GH9. We show that the boosting effect of CgSOD-1 involves an oxidative mechanism of action in which CgSOD-1 generates reactive oxygen species that subsequently cleave the polysaccharide. SOD-type enzymes constitute a new addition to the growing family of oxidases, ones which are up-regulated when exposed to recalcitrant polysaccharides, and that are used by Nature for biomass degradation.

AB - Wood-feeding termites effectively degrade plant biomass through enzymatic degradation. Despite their high efficiencies, however, individual glycoside hydrolases isolated from termites and their symbionts exhibit anomalously low effectiveness in lignocellulose degradation, suggesting hereto unknown enzymatic activities in their digestome. Herein, we demonstrate that an ancient redox-active enzyme encoded by the lower termite Coptotermes gestroi, a Cu/Zn superoxide dismutase (CgSOD-1) plays a previously unknown role in plant biomass degradation. We show that CgSOD-1 transcripts and peptides are up-regulated in response to an increased level of lignocellulose recalcitrance and that CgSOD-1 localizes in the lumen of the fore- and midguts of C. gestroi together with termite main cellulase, CgEG-1-GH9. CgSOD-1 boosts the saccharification of polysaccharides by CgEG-1-GH9. We show that the boosting effect of CgSOD-1 involves an oxidative mechanism of action in which CgSOD-1 generates reactive oxygen species that subsequently cleave the polysaccharide. SOD-type enzymes constitute a new addition to the growing family of oxidases, ones which are up-regulated when exposed to recalcitrant polysaccharides, and that are used by Nature for biomass degradation.

U2 - 10.1039/D1GC04519A

DO - 10.1039/D1GC04519A

M3 - Article

SN - 1463-9262

VL - 24

SP - 4845

EP - 4858

JO - Green Chemistry

JF - Green Chemistry

IS - 12

ER -