title: Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors.
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.
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Firoz
authors.initials: F
authors.lastname: Shah
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: César
authors.initials: C
authors.lastname: Nicolás
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Johan
authors.initials: J
authors.lastname: Bentzer
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Magnus
authors.initials: M
authors.lastname: Ellström
authors.affiliation: Centre for Environmental Sciences, Hasselt University, Building D, Agoralaan, 3590, Diepenbeek, Limburg, Belgium.
authors.forename: Mark
authors.initials: M
authors.lastname: Smits
authors.affiliation: Centre for Environmental Sciences, Hasselt University, Building D, Agoralaan, 3590, Diepenbeek, Limburg, Belgium.
authors.forename: Francois
authors.initials: F
authors.lastname: Rineau
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Björn
authors.initials: B
authors.lastname: Canbäck
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.|Biology Department, Lasry Center for Bioscience, Clark University, 950 Main Street, Worcester, MA, 01610-1477, USA.
authors.forename: Dimitrios
authors.initials: D
authors.lastname: Floudas
authors.affiliation: Centre for Environmental Sciences, Hasselt University, Building D, Agoralaan, 3590, Diepenbeek, Limburg, Belgium.
authors.forename: Robert
authors.initials: R
authors.lastname: Carleer
authors.affiliation: Department of Pharmaceutical Microbiology at the Hans Knöll Institute, Friedrich-Schiller-Universität, Beutenbergstrasse 11a, 07745, Jena, Germany.
authors.forename: Gerald
authors.initials: G
authors.lastname: Lackner
authors.affiliation: Department of Pharmaceutical Microbiology at the Hans Knöll Institute, Friedrich-Schiller-Universität, Beutenbergstrasse 11a, 07745, Jena, Germany.
authors.forename: Jana
authors.initials: J
authors.lastname: Braesel
authors.affiliation: Department of Pharmaceutical Microbiology at the Hans Knöll Institute, Friedrich-Schiller-Universität, Beutenbergstrasse 11a, 07745, Jena, Germany.
authors.forename: Dirk
authors.initials: D
authors.lastname: Hoffmeister
authors.affiliation: Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, Marseille, 13288, France.|Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
authors.forename: Bernard
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.|Bioinformatics Infrastructures for Life Sciences (BILS), Department of Biology, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Dag
authors.initials: D
authors.lastname: Ahrén
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Tomas
authors.initials: T
authors.lastname: Johansson
authors.affiliation: Biology Department, Lasry Center for Bioscience, Clark University, 950 Main Street, Worcester, MA, 01610-1477, USA.
authors.forename: David S
authors.initials: DS
authors.lastname: Hibbett
authors.affiliation: Institut de la Recherche Agronomique (INRA), Laboratory of Excellence ARBRE, UMR INRA-Université de Lorraine 'Interactions Arbres/Micro-organismes', INRA-Nancy, 54280, Champenoux, France.
authors.forename: Francis
authors.identifier: http://orcid.org/0000-0002-4737-3715
authors.initials: F
authors.lastname: Martin
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.|Centre for Environmental and Climate Research (CEC), Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Per
authors.initials: P
authors.lastname: Persson
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
authors.forename: Anders
authors.initials: A
authors.lastname: Tunlid
mesh_terms: D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism; D005658:Fungi / Q000235:genetics / Q000502:physiology*; D015966:Gene Expression Regulation, Fungal; D005800:Genes, Fungal; D042845:Laccase / Q000378:metabolism; D008031:Lignin / Q000378:metabolism; D038821:Mycorrhizae / Q000502:physiology*; D009930:Organic Chemicals / Q000032:analysis*; D010084:Oxidation-Reduction; D010802:Phylogeny; D064210:Secondary Metabolism / Q000235:genetics; D012987:Soil / Q000737:chemistry*; D014158:Transcription, Genetic
chemical_list: D005656:Fungal Proteins; D009930:Organic Chemicals; D012987:Soil; D008031:Lignin; D042845:Laccase
keywords: decomposition; ectomycorrhizal fungi; evolution; soil organic matter; spectroscopy; transcriptome