X-ray scattering reveals two mechanisms of cellulose microfibril degradation by filamentous fungi

Summary, in English

Mushroom-forming fungi (Agaricomycetes)
employ enzymatic and nonenzymatic cellulose degradation mechanisms, the
latter presumably relying on Fenton-generated radicals. The effects of
the two mechanisms on the cellulose microfibrils structure remain poorly
understood. We examined cellulose degradation caused by litter
decomposers and wood decomposers, including brown-rot and white-rot
fungi and one fungus with uncertain wood decay type, by combining small-
and wide-angle X-ray scattering. We also examined the effects of
commercial enzymes and Fenton-generated radicals on cellulose using the
same method. We detected two main degradation or modification
mechanisms. The first characterized the mechanism used by most fungi and
resembled enzymatic cellulose degradation, causing simultaneous
microfibril thinning and decreased crystalline cellulose. The second
mechanism was detected in one brown-rot fungus and one litter decomposer
and was characterized by patchy amorphogenesis of crystalline cellulose
without substantial thinning of the fibers. This pattern did not
resemble the effect of Fenton-generated radicals, suggesting a more
complex mechanism is involved in the destruction of cellulose
crystallinity by fungi. Furthermore, our results showed a mismatch
between decay classifications and cellulose degradation patterns and
that even within litter decomposers two degradation mechanisms were
found, suggesting higher functional diversity under current ecological
classifications of fungi.
IMPORTANCE
Cellulose degradation by fungi plays a fundamental role in terrestrial
carbon cycling, but the mechanisms by which fungi cope with the
crystallinity of cellulose are not fully understood. We used X-ray
scattering to analyze how fungi, a commercial enzyme mix, and a Fenton
reaction-generated radical alter the crystalline structure of cellulose.
Our data revealed two mechanisms involved in crystalline cellulose
degradation by fungi: one that results in the thinning of the cellulose
fibers, resembling the enzymatic degradation of cellulose, and one that
involves amorphogenesis of crystalline cellulose by yet-unknown
pathways, resulting in a patchy-like degradation pattern. These results
pave the way to a deeper understanding of cellulose degradation and the
development of novel ways to utilize crystalline cellulose.