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

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Author(s)

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

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Publication details

JournalGreen Chemistry
DateAccepted/In press - 7 May 2022
DateE-pub ahead of print (current) - 12 May 2022
Early online date12/05/22
Original languageEnglish

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.

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