Insights into the Molecular Mechanisms of Litter Decomposition and Assimilation of Nitrogen by Ectomycorrhizal Fungi
Author
Summary, in English
Ectomycorrhizae is the dominant type of mycorrhiza found in association with tree roots in
boreal and northern temperate forests. In this symbiosis, the fungal partner derives energy from
photosynthates provided by the host trees and in return delivers soil-derived nutrients such as
nitrogen (N). The majority of N in forest soils is embedded in recalcitrant organic matter–protein
complexes. Ectomycorrhizal fungi (EMF) are thought to have a key role in decomposing and
mobilizing nitrogen from such complexes. However, little is known about the mechanisms
governing these decomposing processes, how they are regulated by C and N availability, and the
mechanisms of organic N uptake. The work described in the thesis uses spectroscopic methods,
chemical analysis and transcriptome profiling to examine the mechanisms by which the model
ectomycorrhizal fungus Paxillus involutus degrades soil organic matter (SOM) while assimilating
the organic nitrogen from plant litter. Finally, the decomposing ability of seven other species of
EMF was examined that differ in ecology and evolutionary history.
The EMF P. involutus degraded SOM, while assimilating N, by a radical-based oxidation
involving Fenton chemistry similar to the mechanism used by saprophytic brown-rot (BR) fungi.
The key indications were the apparition of a C=O peak in the signature of cellulose, the side
chain modifications of lignin residues, and the increase in the Fe3+-reducing activity in the culture
filtrate. The set of enzymes expressed during the degradation of SOM was similar to the set of
enzymes involved in the oxidative degradation of wood by BR fungi. Secondary metabolites are
key components for Fe3+-reduction and the generation of Fenton reagent in BR oxidative
degradation of lignocellulose. The Fe3+-reducing activity of P. involutus was caused by the
pigment involutin. The saprotrophic activity of P. involutus is reduced to a radical-based
biodegradation system that efficiently disrupts the organic matter and thereby mobilizes the
entrapped N. The decomposition of plant litter and assimilation of nitrogen was triggered by the
addition of glucose while ammonium addition had minor effects. P. involutus secreted peptidase
activity, mostly contributed by aspartic peptidases while degrading proteins. The expression levels
of extracellular peptidases were regulated in parallel with transporters and enzymes involved in the
assimilation and metabolism of the released peptides and amino acids. Finally, all the examined
EMF species catalyzes oxidative degradation of complex organic components in the litter extract
with a mechanism similar to that of BR fungi. The ability to modify complex organic material by
oxidation is not restricted to rapidly-growing, long-distance exploration types of EMF, but it is
also found in slow-growing, medium- and short-distance EMF exploration types. All examined
EMF species expresses distinctively different sets oxidative enzymes to oxidize the litter material.
Thus, EMF can degrade plant litter by oxidative mechanisms similar to BR while variation in
gene expression might reflect adaptations of the decomposing mechanisms to different
environmental conditions.
boreal and northern temperate forests. In this symbiosis, the fungal partner derives energy from
photosynthates provided by the host trees and in return delivers soil-derived nutrients such as
nitrogen (N). The majority of N in forest soils is embedded in recalcitrant organic matter–protein
complexes. Ectomycorrhizal fungi (EMF) are thought to have a key role in decomposing and
mobilizing nitrogen from such complexes. However, little is known about the mechanisms
governing these decomposing processes, how they are regulated by C and N availability, and the
mechanisms of organic N uptake. The work described in the thesis uses spectroscopic methods,
chemical analysis and transcriptome profiling to examine the mechanisms by which the model
ectomycorrhizal fungus Paxillus involutus degrades soil organic matter (SOM) while assimilating
the organic nitrogen from plant litter. Finally, the decomposing ability of seven other species of
EMF was examined that differ in ecology and evolutionary history.
The EMF P. involutus degraded SOM, while assimilating N, by a radical-based oxidation
involving Fenton chemistry similar to the mechanism used by saprophytic brown-rot (BR) fungi.
The key indications were the apparition of a C=O peak in the signature of cellulose, the side
chain modifications of lignin residues, and the increase in the Fe3+-reducing activity in the culture
filtrate. The set of enzymes expressed during the degradation of SOM was similar to the set of
enzymes involved in the oxidative degradation of wood by BR fungi. Secondary metabolites are
key components for Fe3+-reduction and the generation of Fenton reagent in BR oxidative
degradation of lignocellulose. The Fe3+-reducing activity of P. involutus was caused by the
pigment involutin. The saprotrophic activity of P. involutus is reduced to a radical-based
biodegradation system that efficiently disrupts the organic matter and thereby mobilizes the
entrapped N. The decomposition of plant litter and assimilation of nitrogen was triggered by the
addition of glucose while ammonium addition had minor effects. P. involutus secreted peptidase
activity, mostly contributed by aspartic peptidases while degrading proteins. The expression levels
of extracellular peptidases were regulated in parallel with transporters and enzymes involved in the
assimilation and metabolism of the released peptides and amino acids. Finally, all the examined
EMF species catalyzes oxidative degradation of complex organic components in the litter extract
with a mechanism similar to that of BR fungi. The ability to modify complex organic material by
oxidation is not restricted to rapidly-growing, long-distance exploration types of EMF, but it is
also found in slow-growing, medium- and short-distance EMF exploration types. All examined
EMF species expresses distinctively different sets oxidative enzymes to oxidize the litter material.
Thus, EMF can degrade plant litter by oxidative mechanisms similar to BR while variation in
gene expression might reflect adaptations of the decomposing mechanisms to different
environmental conditions.
Publishing year
2014
Language
English
Document type
Dissertation
Publisher
Department of Biology, Lund University
Topic
- Biological Sciences
Keywords
- Ectomycorrhizal fungi
- Paxillus involutus
- organic matter degradation
- Fenton chemistry
- carbon availability
- N assimilation
- C and N cycling
- protein degradation pathway
- secondary metabolites
Status
Published
Research group
- Microbial Ecology
Supervisor
ISBN/ISSN/Other
- ISBN: 978-91-7473-937-4
Defence date
9 May 2014
Defence time
10:00
Defence place
Blue Hall, Ecology Building, Sölvegatan 37, 223 62 Lund, Sweden
Opponent
- Mika Tarkka (Dr.)