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

Shah, Firoz; Nicolás, César; Bentzer, Johan; Ellström, Magnus; Smits, Mark; Rineau, Francois; Canbäck, Björn; Floudas, Dimitrios; Carleer, Robert; Lackner, Gerald; Braesel, Jana; Hoffmeister, Dirk; Henrissat, Bernard; Ahrén, Dag; Johansson, Tomas; Hibbett, David S.; Martin, Francis; Persson, Per; Tunlid, Anders

doi:10.1111/nph.13722

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

Journal Article · Mon Nov 02 23:00:00 EST 2015 · New Phytologist

DOI:https://doi.org/10.1111/nph.13722· OSTI ID:1625913

Shah, Firoz ^[1]; Nicolás, César ^[2]; Bentzer, Johan ^[2]; Ellström, Magnus ^[2]; Smits, Mark ^[3]; Rineau, Francois ^[3]; Canbäck, Björn ^[2]; Floudas, Dimitrios ^[4]; Carleer, Robert ^[3]; Lackner, Gerald ^[5]; Braesel, Jana ^[5]; Hoffmeister, Dirk ^[5]; Henrissat, Bernard ^[6]; Ahrén, Dag ^[2]; Johansson, Tomas ^[2]; Hibbett, David S. ^[7]; ^[8]; Persson, Per ^[2]; Tunlid, Anders ^[2]

Lund Univ. (Sweden); DOE/OSTI
Lund Univ. (Sweden)
Hasselt Univ., Diepenbeek (Belgium)
Lund Univ. (Sweden); Clark Univ., Worcester, MA (United States)
Friedrich Schiller Univ., Jena (Germany)
Centre National de la Recherche Scientifique (CNRS), Marseille (France); Aix-Marseille Univ., Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
Clark Univ., Worcester, MA (United States)
French National Research Institute for Agriculture, Food and Environment (INRAE), Champenoux (France); Universite de Lorraine, Champenoux (France)

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.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Swedish Research Council (VR); Knut and Alice Wallenberg Foundation (KAWF); French National Research Agency (ANR)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625913

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 209; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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60 APPLIED LIFE SCIENCES
Plant Sciences
decomposition
ectomycorrhizal fungi
evolution
soil organic matter
spectroscopy
transcriptome

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

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