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

Franco Cairo, João Paulo; Mandelli, Fernanda; Tramontina, Robson; Cannella, David; Paradisi, Alessandro; Ciano, Luisa; Ferreira, Marcel; Liberato, Marcelo Vizoná; Brenelli, Lívia; Gonçalves, Thiago; Rodrigues, Gisele Nunes; Alvarez, Thabata Maria; Mofatto, Luciana Souto; Carazzolle, Marcelo Falsarella; Pradella, José Geraldo; Leme, Adriana Paes; Costa-Leonardo, Ana Maria; Oliveira Neto, Mario; Damasio, André; Davies, Gideon; Felby, Claus; Walton, Paul Howard; Squina, Fabio

Abstract

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.

Citation

Franco Cairo, J. P., Mandelli, F., Tramontina, R., Cannella, D., Paradisi, A., Ciano, L., …Squina, F. (2022). Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases. Green Chemistry, 24(12), 4845-4858. https://doi.org/10.1039/d1gc04519a

• Journal Article Type: Article
• Acceptance Date: May 7, 2022
• Online Publication Date: May 12, 2022
• Publication Date: Jun 21, 2022
• Deposit Date: May 20, 2022
• Publicly Available Date: May 24, 2022
• Journal: Green Chemistry
• Print ISSN: 1463-9262
• Electronic ISSN: 1463-9270
• Publisher: Royal Society of Chemistry
• Peer Reviewed: Peer Reviewed
• Volume: 24
• Issue: 12
• Pages: 4845-4858
• DOI: https://doi.org/10.1039/d1gc04519a
• Keywords: Pollution; Environmental Chemistry
• Public URL: https://nottingham-repository.worktribe.com/output/8135502
• Publisher URL: https://pubs.rsc.org/en/Content/ArticleLanding/2022/GC/D1GC04519A