Spatial mapping of extracellular oxidant production by a white rot basidiomycete on wood reveals details of ligninolytic mechanism

Summary Oxidative cleavage of the recalcitrant plant polymer lignin is a crucial step in global carbon cycling, and is accomplished most efficiently by fungi that cause white rot of wood. These basidiomycetes secrete many enzymes and metabolites with proposed ligninolytic roles, and it is not clear...

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Bibliographic Details
Published in:Environmental microbiology 2013-03, Vol.15 (3), p.956-966
Main Authors: Hunt, Christopher G., Houtman, Carl J., Jones, Don C., Kitin, Peter, Korripally, Premsagar, Hammel, Kenneth E.
Format: Article
Language:English
Subjects:
Animal, plant and microbial ecology
Basidiomycetes
Benzyl Alcohols - chemistry
Biological and medical sciences
Fundamental and applied biological sciences. Psychology
Fungi
General aspects
Half-Life
Hyphae - metabolism
Lignin - metabolism
Microbial ecology
Microbiology
Miscellaneous
Mycology
Oxidants - biosynthesis
Oxidants - metabolism
Phanerochaete - chemistry
Phanerochaete - genetics
Phanerochaete - metabolism
Phanerochaete chrysosporium
Wood - microbiology
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Summary:Summary Oxidative cleavage of the recalcitrant plant polymer lignin is a crucial step in global carbon cycling, and is accomplished most efficiently by fungi that cause white rot of wood. These basidiomycetes secrete many enzymes and metabolites with proposed ligninolytic roles, and it is not clear whether all of these agents are physiologically important during attack on natural lignocellulosic substrates. One new approach to this problem is to infer properties of ligninolytic oxidants from their spatial distribution relative to the fungus on the lignocellulose. We grew Phanerochaete chrysosporium on wood sections in the presence of oxidant‐sensing beads based on the ratiometric fluorescent dye BODIPY 581/591. The beads, having fixed locations relative to the fungal hyphae, enabled spatial mapping of cumulative extracellular oxidant distributions by confocal fluorescence microscopy. The results showed that oxidation gradients occurred around the hyphae, and data analysis using a mathematical reaction–diffusion model indicated that the dominant oxidant during incipient white rot had a half‐life under 0.1 s. The best available hypothesis is that this oxidant is the cation radical of the secreted P. chrysosporium metabolite veratryl alcohol.
ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.12039