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X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi

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 degradatio...

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Autores principales: Floudas, Dimitrios, Gentile, Luigi, Andersson, Erika, Kanellopoulos, Spyros G., Tunlid, Anders, Persson, Per, Olsson, Ulf
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9469724/
https://www.ncbi.nlm.nih.gov/pubmed/35997493
http://dx.doi.org/10.1128/aem.00995-22
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author Floudas, Dimitrios
Gentile, Luigi
Andersson, Erika
Kanellopoulos, Spyros G.
Tunlid, Anders
Persson, Per
Olsson, Ulf
author_facet Floudas, Dimitrios
Gentile, Luigi
Andersson, Erika
Kanellopoulos, Spyros G.
Tunlid, Anders
Persson, Per
Olsson, Ulf
author_sort Floudas, Dimitrios
collection PubMed
description 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.
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spelling pubmed-94697242022-09-14 X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi Floudas, Dimitrios Gentile, Luigi Andersson, Erika Kanellopoulos, Spyros G. Tunlid, Anders Persson, Per Olsson, Ulf Appl Environ Microbiol Environmental Microbiology 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. American Society for Microbiology 2022-08-23 /pmc/articles/PMC9469724/ /pubmed/35997493 http://dx.doi.org/10.1128/aem.00995-22 Text en Copyright © 2022 Floudas et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Environmental Microbiology
Floudas, Dimitrios
Gentile, Luigi
Andersson, Erika
Kanellopoulos, Spyros G.
Tunlid, Anders
Persson, Per
Olsson, Ulf
X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi
title X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi
title_full X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi
title_fullStr X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi
title_full_unstemmed X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi
title_short X-Ray Scattering Reveals Two Mechanisms of Cellulose Microfibril Degradation by Filamentous Fungi
title_sort x-ray scattering reveals two mechanisms of cellulose microfibril degradation by filamentous fungi
topic Environmental Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9469724/
https://www.ncbi.nlm.nih.gov/pubmed/35997493
http://dx.doi.org/10.1128/aem.00995-22
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