Oxidative damage control during decay of wood by brown rot fungus using oxygen radicals

Jesus D. Castaño, Jiwei Zhang, Claire E. Anderson, Jonathan S. Schilling

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Brown rot wood-degrading fungi deploy reactive oxygen species (ROS) to loosen plant cell walls and enable selective polysaccharide extraction. These ROS, including Fenton-generated hydroxyl radicals (HO), react with little specificity and risk damaging hyphae and secreted enzymes. Recently, it was shown that brown rot fungi reduce this risk, in part, by differentially expressing genes involved in HO generation ahead of those coding carbohydrate-active enzymes (CAZYs). However, there are notable exceptions to this pattern, and we hypothesized that brown rot fungi would require additional extracellular mechanisms to limit ROS damage. To assess this, we grew Postia placenta directionally on wood wafers to spatially segregate early from later decay stages. Extracellular HO production (avoidance) and quenching (suppression) capacities among the stages were analyzed, along with the ability of secreted CAZYs to maintain activity postoxidation (tolerance). First, we found that H2O2 and Fe2+ concentrations in the extracellular environment were conducive to HO production in early (H2O2:Fe2+ ratio 2:1) but not later (ratio 1:131) stages of decay. Second, we found that ABTS radical cation quenching (antioxidant capacity) was higher in later decay stages, coincident with higher fungal phenolic concentrations. Third, by surveying enzyme activities before/after exposure to Fenton-generated HO, we found that CAZYs secreted early, amid HO, were more tolerant of oxidative stress than those expressed later and were more tolerant than homologs in the model CAZY producer Trichoderma reesei. Collectively, this indicates that P. placenta uses avoidance, suppression, and tolerance mechanisms, extracellularly, to complement intracellular differential expression, enabling this brown rot fungus to use ROS to degrade wood.

Original languageEnglish (US)
Article numbere01937-18
JournalApplied and environmental microbiology
Volume84
Issue number22
DOIs
StatePublished - Nov 1 2018

Keywords

  • Antioxidant capacity
  • Fenton reaction
  • Glycosyl hydrolases
  • Hydroxyl radicals
  • Oxidative stress tolerance
  • Wood decay

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