Ectomycorrhizal fungi decompose humus-rich litter material using oxidative mechanisms adapted from saprotrophic ancestors
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PROVIDER: PRJNA272430 | ENA |
REPOSITORIES: ENA
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Project description:Decomposition of soil organic matter in forest soils is thought to be controlled by the activity of saprotrophic fungi, while biotrophic fungi including ectomycorrhizal fungi act as vectors for input of plant carbon. The limited decomposing ability of ectomycorrhizal fungi is supported by recent findings showing that they have lost many of the genes that encode hydrolytic plant cell-wall degrading enzymes in their saprophytic ancestors. Nevertheless, here we demonstrate that ectomycorrhizal fungi representing at least four origins of symbiosis have retained significant capacity to degrade humus-rich litter amended with glucose. Spectroscopy showed that this decomposition involves an oxidative mechanism and that the extent of oxidation varies with the phylogeny and ecology of the species. RNA-Seq analyses revealed that the genome-wide set of expressed transcripts during litter decomposition has diverged over evolutionary time. Each species expressed a unique set of enzymes that are involved in oxidative lignocellulose degradation by saprotrophic fungi. A comparison of closely related species within the Boletales showed that ectomycorrhizal fungi oxidized litter material as efficiently as brown-rot saprotrophs. The ectomycorrhizal species within this clade exhibited more similar decomposing mechanisms than expected from the species phylogeny in concordance with adaptive evolution occurring as a result of similar selection pressures. Our data shows that ectomycorrhizal fungi are potential organic matter decomposers, yet not saprotrophs. We suggest that the primary function of this decomposing activity is to mobilize nutrients embedded in organic matter complexes and that the activity is driven by host carbon supply. Comparative transcriptomics of ectomycorrhizal (ECM) versus brown-rot (BR) fungi while degrading soil-organic matter
2015-09-24 | E-GEOD-64897 | biostudies-arrayexpress
Project description:Decomposition of soil organic matter in forest soils is thought to be controlled by the activity of saprotrophic fungi, while biotrophic fungi including ectomycorrhizal fungi act as vectors for input of plant carbon. The limited decomposing ability of ectomycorrhizal fungi is supported by recent findings showing that they have lost many of the genes that encode hydrolytic plant cell-wall degrading enzymes in their saprophytic ancestors. Nevertheless, here we demonstrate that ectomycorrhizal fungi representing at least four origins of symbiosis have retained significant capacity to degrade humus-rich litter amended with glucose. Spectroscopy showed that this decomposition involves an oxidative mechanism and that the extent of oxidation varies with the phylogeny and ecology of the species. RNA-Seq analyses revealed that the genome-wide set of expressed transcripts during litter decomposition has diverged over evolutionary time. Each species expressed a unique set of enzymes that are involved in oxidative lignocellulose degradation by saprotrophic fungi. A comparison of closely related species within the Boletales showed that ectomycorrhizal fungi oxidized litter material as efficiently as brown-rot saprotrophs. The ectomycorrhizal species within this clade exhibited more similar decomposing mechanisms than expected from the species phylogeny in concordance with adaptive evolution occurring as a result of similar selection pressures. Our data shows that ectomycorrhizal fungi are potential organic matter decomposers, yet not saprotrophs. We suggest that the primary function of this decomposing activity is to mobilize nutrients embedded in organic matter complexes and that the activity is driven by host carbon supply.
2015-09-24 | GSE64897 | GEO
Project description:Many trees form ectomycorrhizal symbiosis with fungi. During symbiosis, the tree roots supply sugar to the fungi in exchange for nitrogen, and this process is critical for the nitrogen and carbon cycles in forest ecosystems. However, the extents to which ectomycorrhizal fungi can liberate nitrogen and modify the soil organic matter and the mechanisms by which they do so remain unclear since they have lost many enzymes for litter decomposition that were present in their free-living, saprotrophic ancestors. Using time-series spectroscopy and transcriptomics, we examined the ability of two ectomycorrhizal fungi from two independently evolved ectomycorrhizal lineages to mobilize soil organic nitrogen. Both species oxidized the organic matter and accessed the organic nitrogen. The expression of those events was controlled by the availability of glucose and inorganic nitrogen. Despite those similarities, the decomposition mechanisms, including the type of genes involved as well as the patterns of their expression, differed markedly between the two species. Our results suggest that in agreement with their diverse evolutionary origins, ectomycorrhizal fungi use different decomposition mechanisms to access organic nitrogen entrapped in soil organic matter. The timing and magnitude of the expression of the decomposition activity can be controlled by the below-ground nitrogen quality and the above-ground carbon supply.
2018-11-30 | GSE110485 | GEO
Project description:Abstract: A large part of the nitrogen in forest soils is found in recalcitrant organic matter-protein complexes. Ectomycorrhizal fungi are thought to have a key role in the decomposition and mobilization of nitrogen from such complexes. The knowledge on the functional mechanisms of these processes, and how they are regulated by carbon from the host plant and the availability of more easily available forms of nitrogen sources are limited. We used spectroscopic analyses and transcriptome profiling to examine how the presence/absence of glucose and ammonium regulates the decomposition and mobilization of nitrogen from litter material by the ectomycorrhizal fungus Paxillus involutus. Amendments of glucose triggered the assimilation of nitrogen and the decomposition of the litter material. Concomitantly, the expression of genes encoding enzymes involved in oxidative (i.e. Fenton chemistry) degradation of polysaccharides and polyphenols, peptidases, nitrogen transporters and enzymes in pathways of the nitrogen and carbon metabolism were upregulated in concert. Addition of ammonium had minute effects on both the expression of transcripts and decomposition of litter material, and only when glucose was present. Based on the spectroscopic analyses, three major types of chemical modifications of the litter material were observed. Each of them was correlated with the expression of specific sets of genes encoding extracellular enzymes. Our data suggests that the expression of the decomposition and nitrogen assimilation machinery of ectomycorrhizal fungi can be firmly regulated by the host carbon supply, i.e. priming, and that the availability of inorganic nitrogen as such has limited effects on the saprotrophic activities. Rineau F, Shah F., Smits M.M., Persson P., Johansson T., Carleer R., Troein C., Tunlid A. (2013) Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus (submitted)
2013-04-30 | GSE45303 | GEO
Project description:Abstract: A large part of the nitrogen in forest soils is found in recalcitrant organic matter-protein complexes. Ectomycorrhizal fungi are thought to have a key role in the decomposition and mobilization of nitrogen from such complexes. The knowledge on the functional mechanisms of these processes, and how they are regulated by carbon from the host plant and the availability of more easily available forms of nitrogen sources are limited. We used spectroscopic analyses and transcriptome profiling to examine how the presence/absence of glucose and ammonium regulates the decomposition and mobilization of nitrogen from litter material by the ectomycorrhizal fungus Paxillus involutus. Amendments of glucose triggered the assimilation of nitrogen and the decomposition of the litter material. Concomitantly, the expression of genes encoding enzymes involved in oxidative (i.e. Fenton chemistry) degradation of polysaccharides and polyphenols, peptidases, nitrogen transporters and enzymes in pathways of the nitrogen and carbon metabolism were upregulated in concert. Addition of ammonium had minute effects on both the expression of transcripts and decomposition of litter material, and only when glucose was present. Based on the spectroscopic analyses, three major types of chemical modifications of the litter material were observed. Each of them was correlated with the expression of specific sets of genes encoding extracellular enzymes. Our data suggests that the expression of the decomposition and nitrogen assimilation machinery of ectomycorrhizal fungi can be firmly regulated by the host carbon supply, i.e. priming, and that the availability of inorganic nitrogen as such has limited effects on the saprotrophic activities. Rineau F, Shah F., Smits M.M., Persson P., Johansson T., Carleer R., Troein C., Tunlid A. (2013) Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus (submitted) A one-chip study (data from 12 subarrays collected from a 12-plex Nimblegen microarray (ID 467991) using total RNA recovered from three separate glass-bead cultures of Paxillus involutus (ATCC200175) after amendments of various soil-derived substrates. Transcriptome profiling to examine how the presence/absence of glucose and ammonium regulates the decomposition and mobilization of nitrogen from litter material by the ectomycorrhizal fungus Paxillus involutus.
2013-04-30 | E-GEOD-45303 | biostudies-arrayexpress
Project description:In this study, examinations were performed on how the ECM fungus Paxillus involutus degrade complex, plant and litter material by using elemental analyses, FTIR spectroscopy, pyrolysis-GC/MS, and synchronous fluorescence spectroscopy together with microarray analyses screening 12,214 gene models, derived from 454 sequenced cDNA libraries. Rineau, F., Roth, D., Shah, F., Smits, M., Johansson, T., Canbäck, B., Bjarke Olsen, P., Persson, P., Nedergaard Grell, M., Lange, L., & Tunlid, A. (201X) Expression levels tune enzymatic exploitation of plant litter material by ectomycorrhizal fungi (manuscript in preparation).
2012-02-01 | GSE34402 | GEO
Project description:Ectomycorrhizal fungi are thought to have a key role in mobilizing organic nitrogen that is trapped in soil organic matter (SOM). However, the extent to which ectomycorrhizal fungi decompose SOM and the mechanism by which they do so remain unclear, considering that they have lost many genes encoding lignocellulose-degrading enzymes that are present in their saprotrophic ancestors. Spectroscopic analyses and transcriptome profiling were used to examine the mechanisms by which five species of ectomycorrhizal fungi, representing at least four origins of symbiosis, decompose SOM extracted from forest soils. In the presence of glucose and when acquiring nitrogen, all species converted the organic matter in the SOM extract using oxidative mechanisms. The transcriptome expressed during oxidative decomposition has diverged over evolutionary time. Each species expressed a different set of transcripts encoding proteins associated with oxidation of lignocellulose by saprotrophic fungi. The decomposition 'toolbox' has diverged through differences in the regulation of orthologous genes, the formation of new genes by gene duplications, and the recruitment of genes from diverse but functionally similar enzyme families. The capacity to oxidize SOM appears to be common among ectomycorrhizal fungi. We propose that the ancestral decay mechanisms used primarily to obtain carbon have been adapted in symbiosis to scavenge nutrients instead.
| S-EPMC5061094 | biostudies-literature
Project description:Ectomycorrhizal fungi are dependent on host trees for carbon supply. In return ectomycorrhizal fungi supply trees with water and nutrients. It is known that when ectomycorrhizal fungi have exploited a nutrient rich patch in soil, the carbon allocation to mycelia in that patch is reduced, with the consequence of mycelia dying, but less is known of the dynamics of this senescence. We cultivated the ectomycorrhizal fungus Paxillus involutus in an axenic system. We collected growth and transcriptome data at different stages of carbon starvation during fungal growth. Carbon starvation induced a decrease in fungal biomass, which coincided with the release of NH4+ and the expression of genes connected with autophagy as well as protease and chitinase activity. Monoaromatic compounds, chitin and protease activity was detected in the liquid growth media during carbon starvation. The exudation of NH4+ and increase of monoaromatic compound during C starvation suggests senescence and autolysis of P. involutus. Together with the upregulation of genes involved in autophagy, chitinase and endopeptidase activity this points towards a controlled senescence including recycling of compounds originating from the fungi. Reduced C allocation to ectomycorrhizal mycelia in recently depleted nutrient patches in forest soils must be of ubiquitous nature. Understanding the mechanisms during exploitation of nutrients by ectomycorrhizal fungi is of great importance for understanding carbon and nutrient dynamics in forest soils. This is to our knowledge the first study describing the carbon starvation response in an ectomycorrhizal fungus.
2014-04-01 | GSE54940 | GEO
Project description:In order to get insights into the ability of ectomycorrhizal fungi to perceive their biotic environment as well as into the mechanisms of the interactions between ectomycorrhizal fungi and soil bacteria, we analysed the transcriptomic response of the ectomycorrhizal fungus L. bicolor and the strain Pseudomonas fluorescens Pf29Arp during their interactions in vitro.
2014-10-01 | GSE55147 | GEO