Aspects Determining the Dominance of Fomitopsis pinicola in the Colonization of Deadwood and the Role of the Pathogenicity Factor Oxalate

Abstract

Carbon and mineral cycling in sustainable forest systems depends on a microbiome of basidiomycetes, ascomycetes, litter-degrading saprobes, ectomycorrhizal, and mycoparasitic fungi that constitute a deadwood degrading consortium. The brown rot basidiomycete Fomitopsis pinicola (Swartz: Fr.) P. Karsten (Fp), as an oxalate-producing facultative pathogen, is an early colonizer of wounded trees and fresh deadwood. It replaces basidiomycetous white rot fungi and non-basidiomycetous fungal phyla in the presence of its volatilome, but poorly in its absence. With the goal of determining its dominance over the most competitive basidiomycetes and its role in fungal successions within the forest microbiome in general, Fp was exposed to the white rot fungus Kuehneromyces mutabilis (Schaeff.: Fr.) Singer & Smith (Km) in aseptic dual culture established on fertilized 100 mm-long wood dust columns in glass tubes with the inclusion of their volatilomes. For the mycelia approaching from the opposite ends of the wood dust columns, the energy-generating systems of laccase and manganese peroxidase (MnP), the virulence factor oxalate, and the exhalation of terpenes were determined by spectrophotometry, High Pressure Liquid Chromatography (HPLC), and Gas Chromatography-Mass Spectrometry (GC-MS). Km mycelia perceived the approaching Fp over 20 mm of non-colonized wood dust, reduced the laccase activity to 25%, and raised MnP to 275%–500% by gaining energy and presumably by controlling oxalate, H2O2, and the dropping substrate pH caused by Fp. On mycelial contact, Km stopped Fp, secured its substrate sector with 4 mm of an impermeable barrier region during an eruption of antimicrobial bisabolenes, and dropped from the invasion mode of substrate colonization into the steady state mode of low metabolic and defensive activity. The approaching Fp raised the oxalate production throughout to >20 g kg−1 to inactivate laccase and caused, with pH 1.4–1.7, lethal conditions in its substrate sector whose physiological effects on Km could be reproduced with acidity conditions incited by HCl. After a mean lag phase of 11 days, Fp persisting in a state of high metabolic activity overgrew and digested the debilitated Km thallus and terminated the production of oxalate. It is concluded that the factors contributing to the competitive advantage of F. pinicola in the colonization of wounded trees and pre-infected deadwood are the drastic long-term acidification of the timber substrate, its own insensitivity to extremely low pH conditions, its efficient control of the volatile mono- and sesquiterpenes of timber and microbial origin, and the action of a undefined blend of terpenes and allelopathic substances.