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New Phytol. 2016 Mar;209(4):1705-19. doi: 10.1111/nph.13722. Epub 2015 Nov 3.

Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors.

Author information

1
Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
2
Centre for Environmental Sciences, Hasselt University, Building D, Agoralaan, 3590, Diepenbeek, Limburg, Belgium.
3
Biology Department, Lasry Center for Bioscience, Clark University, 950 Main Street, Worcester, MA, 01610-1477, USA.
4
Department of Pharmaceutical Microbiology at the Hans Knöll Institute, Friedrich-Schiller-Universität, Beutenbergstrasse 11a, 07745, Jena, Germany.
5
Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, Marseille, 13288, France.
6
Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
7
Bioinformatics Infrastructures for Life Sciences (BILS), Department of Biology, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
8
Institut de la Recherche Agronomique (INRA), Laboratory of Excellence ARBRE, UMR INRA-Université de Lorraine 'Interactions Arbres/Micro-organismes', INRA-Nancy, 54280, Champenoux, France.
9
Centre for Environmental and Climate Research (CEC), Lund University, Ecology Building, SE-223 62, Lund, Sweden.

Abstract

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.

KEYWORDS:

decomposition; ectomycorrhizal fungi; evolution; soil organic matter; spectroscopy; transcriptome

PMID:
26527297
PMCID:
PMC5061094
DOI:
10.1111/nph.13722
[Indexed for MEDLINE]
Free PMC Article

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