A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
- Bioproducts and Biosystems Engineering, University of Minnesota, Saint Paul, Minnesota, USA, Marine and Coastal Research Institute, Invemar, Santa Marta, Colombia
- Bioproducts and Biosystems Engineering, University of Minnesota, Saint Paul, Minnesota, USA
- Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA
- Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
- Plant and Microbial Biology, University of Minnesota, Saint Paul, Minnesota, USA
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.
- Research Organization:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Organization:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Colombian Ministry of Science, Technology, and Innovation
- Grant/Contract Number:
- Biological and Ecological Research program grants DE-SC0019427 and DE-SC0012742; User Facility award EUP50799; SC0012742; SC0019427; EUP50799
- OSTI ID:
- 1813629
- Alternate ID(s):
- OSTI ID: 1904461
- Journal Information:
- mBio (Online), Journal Name: mBio (Online) Vol. 12 Journal Issue: 4; ISSN 2150-7511
- Publisher:
- American Society for MicrobiologyCopyright Statement
- Country of Publication:
- United States
- Language:
- English
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