A fungal secretome adapted for stress enabled a radical wood decay mechanism

Jesus Castaño, Jiwei Zhang, Mowei Zhou, Chia Feng Tsai, Joon Yong Lee, Carrie Nicora, Jonathan Schilling

Research output: Contribution to journalArticlepeer-review

Abstract

Brown rot fungi release massive amounts of carbon from forest deadwood, particularly at high latitudes. These fungi degrade wood by generating small reactive oxygen species (ROS) to loosen lignocellulose, to then selectively remove carbohydrates. The ROS mechanism has long been considered the key adaptation defining brown rot wood decomposition, but recently, we found preliminary evidence that fungal glycoside hydrolases (GHs) implicated in early cell wall loosening might have been adapted to tolerate ROS stress and to synergize with ROS to loosen woody lignocellulose. In the current study, we found more specifically that side chain hemicellulases that help in the early deconstruction of the lignocellulosic complex are significantly more tolerant of ROS in the brown rot fungus Rhodonia placenta than in a white rot fungus (Trametes versicolor) and a soft rot fungus (Trichoderma reesei). Using proteomics to understand the extent of tolerance, we found that significant oxidation of secreted R. placenta proteins exposed to ROS was less than half of the oxidation observed for T. versicolor or T. reesei. The principal oxidative modifications observed in all cases were monooxidation and dioxidation/trioxidation (mainly in methionine and tryptophan residues), some of which were critical for enzyme activity. At the peptide level, we found that GHs in R. placenta were the least ROS affected among our tested fungi. These results confirm and describe underlying mechanisms of tolerance in early-secreted brown rot fungal hemicellulases. These enzymatic adaptations may have been as important as nonenzymatic ROS pathway adaptations in brown rot fungal evolution. IMPORTANCE Brown rot fungi play a critical role in carbon recycling and are of industrial interest. These fungi typically use reactive oxygen species (ROS) to indiscriminately "loosen" wood cell walls at the outset of decay. Brown rot fungi avoid oxidative stress associated with this ROS step by delaying the expression/secretion of many carbohydrate-active enzymes, but there are exceptions, notably some side chain hemicellulases, implicated in loosening lignocellulose. In this study, we provide enzyme activity and secretomic evidence that these enzymes in the brown rot model Rhodonia placenta are more ROS tolerant than the white and soft rot isolates tested. For R. placenta, and perhaps all brown rot lineages, these ROS tolerance adaptions may have played a long-overshadowed role in enabling brown rot.

Original languageEnglish (US)
Article numbere02040-21
JournalmBio
Volume12
Issue number4
DOIs
StatePublished - Aug 2021

Bibliographical note

Funding Information:
We thank the Fulbright Commission and the Colombian Ministry of Science, Technology, and Innovation for the funding of J.C. We gratefully acknowledge funding support from U.S. Department of Energy Biological and Environmental Research program grants DE-SC0019427 and DE-SC0012742 and user facility award EUP50799, each awarded to J.S. as the principal investigator.

Publisher Copyright:
© 2021 Castaño et al.

Keywords

  • Brown rot fungi
  • Glycosyl hydrolases
  • Proteomics
  • ROS tolerance

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, Non-U.S. Gov't

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