Profiles of enzyme activities, production of oxalic acid, and Fe3+-reducing metabolites secreted by the Polyporales brown-rot species Fomitopsis pinicola

2018 
Basidiomycota fungi in the order Polyporales are specified to decomposition of dead wood and woody debris, and thereby, are crucial players in degradation of organic matter and cycling of carbon in the forest ecosystems. Polyporales wood-decaying species comprise of both white-rot and brown-rot fungi, based on their mode of wood decay. While the white-rot fungi are able to attack and decompose all the lignocellulose biopolymers, the brown-rot species mainly cause destruction of wood polysaccharides with minor modification of the lignin units. The biochemical mechanism of brown-rot decay of wood is still unclear, and has been proposed to include a combination of non-enzymatic oxidation reactions and carbohydrate-active enzymes. Therefore, a linking approach is needed to dissect the fungal brown-rot processes. We studied the brown-rot Polyporales species Fomitopsis pinicola , by following mycelial growth and enzyme activity patterns, and generation of metabolites together with Fenton promoting Fe 3+ -reducing activity, for three months in submerged cultures supplemented with spruce wood. Enzyme activities to degrade hemicellulose, cellulose, proteins and chitin were produced by three Finnish isolates of F. pinicola . Substantial secretion of oxalic acid and decrease in pH were notable. Aromatic compounds and metabolites were observed to accumulate in the fungal cultures, with some metabolites having Fe 3+ -reducing activity. Thus, F. pinicola demonstrates a pattern of strong mycelial growth leading to active production of carbohydrate and protein-active enzymes, together with promotion of Fenton biochemistry. Our findings point to fungal species-level “fine-tuning” and variations in the biochemical reactions leading to brown-rot type of decay of wood. Importance Fomitopsis pinicola is a common fungal species in boreal and temperate forests in the northern hemisphere encountered as a wood-colonizing saprotroph and tree pathogen, causing a severe brown-rot type of degradation of wood. However, its lignocellulose-decomposing mechanisms have remained undiscovered. Our approach was to explore both the enzymatic activities, and non-enzymatic Fenton reaction promoting activities (Fe 3+ -reduction, metabolite production), by cultivating three isolates of F. pinicola in wood-supplemented cultures. Our findings on the simultaneous production of versatile enzyme activities, including endoglucanase, xylanase, β-glucosidase, chitinase, and acid peptidase, together with generation of low pH, accumulation of oxalic acid and Fe 3+ -reducing metabolites, open up the variations of fungal brown-rot decay mechanisms. Furthermore, these findings will aid us in revealing the wood-decay proteome, transcriptome and metabolic activities of this ecologically important forest fungal species.
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