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Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.19471· OSTI ID:2473667
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  1. Universite de Lorraine, Nancy (France); French National Research Institute for Agriculture, Food and Environment (INRAE), Nancy (France)
  2. Centre National de la Recherche Scientifique (CNRS), Marseille (France); Aix-Marseille Univ., Marseille (France); French National Research Institute for Agriculture, Food and Environment (INRAE), Marseille (France)
  3. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  4. Natural Resources Canada, Quebec, QC (Canada). Canadian Forest Service
  5. Public University of Navarra (UPNA), Pamplona (Spain)
  6. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden)
  7. Technical Univ. of Denmark, Copenhagen (Denmark); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  8. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)

Soil fungi belonging to different functional guilds, such as saprotrophs, pathogens, and mycorrhizal symbionts, play key roles in forest ecosystems. To date, no study has compared the actual gene expression of these guilds in different forest soils. We used metatranscriptomics to study the competition for organic resources by these fungal groups in boreal, temperate, and Mediterranean forest soils. Using a dedicated mRNA annotation pipeline combined with the JGI MycoCosm database, we compared the transcripts of these three fungal guilds, targeting enzymes involved in C- and N mobilization from plant and microbial cell walls. Genes encoding enzymes involved in the degradation of plant cell walls were expressed at a higher level in saprotrophic fungi than in ectomycorrhizal and pathogenic fungi. However, ectomycorrhizal and saprotrophic fungi showed similarly high expression levels of genes encoding enzymes involved in fungal cell wall degradation. Transcripts for N-related transporters were more highly expressed in ectomycorrhizal fungi than in other groups. Here, we showed that ectomycorrhizal and saprotrophic fungi compete for N in soil organic matter, suggesting that their interactions could decelerate C cycling. Metatranscriptomics provides a unique tool to test controversial ecological hypotheses and to better understand the underlying ecological processes involved in soil functioning and carbon stabilization.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); Spanish National Research Agency (CICYT)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2473667
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 242; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (98)

Boreal tree species change as a climate mitigation strategy: impact on ecosystem C and N stocks and soil nutrient levels journal November 2021
Linking Genes to Traits in Fungi journal January 2021
Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi journal January 2007
Diversity of leaf litter leachates from temperate forest trees and its consequences for soil microbial activity journal August 2016
FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles journal November 2020
Impact of forest thinning on aboveground macrofungal community composition and diversity in Mediterranean pine stands journal December 2021
Characterization and regulation of PiDur3, a permease involved in the acquisition of urea by the ectomycorrhizal fungus Paxillus involutus journal June 2008
Influence of tree species on richness and diversity of epigeous fungal communities in a French temperate forest stand journal February 2011
Selection and validation of enzymatic activities as functional markers in wood biotechnology and fungal ecology journal February 2013
Plant adaptations to severely phosphorus-impoverished soils journal June 2015
Root associated fungi respond more strongly than rhizosphere soil fungi to N fertilization in a boreal forest journal April 2021
Diversity of laccase genes from basidiomycetes in a forest soil journal July 2004
Diversity of bacterial laccase-like multicopper oxidase genes in forest and grassland Cambisol soil samples journal March 2008
Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect journal January 2011
Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition journal February 2013
Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry journal September 2015
Tree species select diverse soil fungal communities expressing different sets of lignocellulolytic enzyme-encoding genes journal September 2016
Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter journal May 2021
Leaf manganese accumulation and phosphorus-acquisition efficiency journal February 2015
Mycorrhiza and Litter Decomposition journal September 1971
Soil eukaryotic functional diversity, a metatranscriptomic approach journal September 2007
Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants journal July 2013
Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses journal August 2012
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists journal February 2015
Fast and sensitive protein alignment using DIAMOND journal November 2014
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen journal December 2018
Comparative genomics reveals the origin of fungal hyphae and multicellularity journal September 2019
Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits journal October 2020
Tree functional traits, forest biomass, and tree species diversity interact with site properties to drive forest soil carbon journal March 2022
Function and functional redundancy in microbial systems journal April 2018
Environment and host as large-scale controls of ectomycorrhizal fungi journal June 2018
Structure and function of the global topsoil microbiome journal August 2018
Ericoid mycorrhizal fungi are common root associates of a Mediterranean ectomycorrhizal plant ( Quercus ilex ) journal October 2000
Excretion of two proteases by the ectomycorrhizal fungus Amanita muscaria: Protease excretion by ectomycorrhizal fungus Amanita muscaria journal July 2001
Dominant species maintain ecosystem function with non-random species loss journal June 2003
Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil journal June 2002
Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests journal June 2022
Forest Fertilization Research in Finland: A Literature Review journal January 2001
The Sequence Alignment/Map format and SAMtools journal June 2009
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
The carbohydrate-active enzyme database: functions and literature journal November 2021
Database resources of the national center for biotechnology information journal December 2021
GenBank journal November 2012
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
MEROPS : the database of proteolytic enzymes, their substrates and inhibitors journal October 2013
Historical Patterns of Forest Fertilization in the Southeastern United States from 1969 to 2004 journal August 2007
Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently journal May 2016
Links between boreal forest management, soil fungal communities and below‐ground carbon sequestration journal December 2021
Deconstructing the microbial necromass continuum to inform soil carbon sequestration journal February 2022
Crown‐fire severity is more important than ground‐fire severity in determining soil fungal community development in the boreal forest journal November 2020
Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with P iloderma- P inus symbiosis: improved methodologies for assessing gene expression in situ : Metatranscriptomic analysis of ectomycorrhizae journal October 2014
Compartmentalized and contrasted response of ectomycorrhizal and soil fungal communities of Scots pine forests along elevation gradients in France and Spain journal June 2015
Functional outcomes of fungal community shifts driven by tree genotype and spatial-temporal factors in Mediterranean pine forests journal March 2017
Fungal ecological strategies reflected in gene transcription ‐ a case study of two litter decomposers journal August 2019
A global synthesis and conceptualization of the magnitude and duration of soil carbon losses in response to forest disturbances journal October 2023
Spatial structure and the effects of host and soil environments on communities of ectomycorrhizal fungi in wooded savannas and rain forests of Continental Africa and Madagascar: AFRICAN ECTOMYCORRHIZAL FUNGI journal June 2011
Occurrence of N‐acetylhexosaminidase‐encoding genes in ectomycorrhizal basidiomycetes journal July 2004
Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests: Methods journal March 2005
Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest journal November 2006
Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen journal March 2012
Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas journal April 1998
Genome‐based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles journal February 2019
Parallel metatranscriptome analysis reveals degradation of plant secondary metabolites by beetles and their gut symbionts journal June 2022
Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function journal October 2013
Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs journal December 2014
Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? journal September 2015
Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus journal January 2018
Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists journal January 2018
Soil microclimate changes affect soil fungal communities in a Mediterranean pine forest journal May 2018
Exploring the role of ectomycorrhizal fungi in soil carbon dynamics journal February 2019
Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition journal November 2019
Transcriptional acclimation and spatial differentiation characterize drought response by the ectomycorrhizal fungus Suillus pungens journal November 2021
Shift in tree species changes the belowground biota of boreal forests journal April 2022
Functional genomics gives new insights into the ectomycorrhizal degradation of chitin journal February 2023
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes journal June 2012
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest journal March 2013
Soil Fungal Cellobiohydrolase I Gene ( cbhI ) Composition and Expression in a Loblolly Pine Plantation under Conditions of Elevated Atmospheric CO 2 and Nitrogen Fertilization journal March 2012
Fungal Traits That Drive Ecosystem Dynamics on Land journal May 2015
Distinct Biogeographic Patterns for Archaea, Bacteria, and Fungi along the Vegetation Gradient at the Continental Scale in Eastern China journal February 2017
Comparative Fungal Community Analyses Using Metatranscriptomics and Internal Transcribed Spacer Amplicon Sequencing from Norway Spruce journal February 2021
Transcriptional Landscape of Ectomycorrhizal Fungi and Their Host Provides Insight into N Uptake from Forest Soil journal February 2022
Wood decomposition, higher fungi, and their role in nutrient redistribution journal December 1995
Evolution of the Mode of Nutrition in Symbiotic and Saprotrophic Fungi in Forest Ecosystems journal November 2021
Mycorrhizal Fungi as Mediators of Soil Organic Matter Dynamics journal November 2019
Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life journal September 2017
ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases journal January 2010
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome journal January 2009
Transcriptional profile of oil palm pathogen, Ganoderma boninense, reveals activation of lignin degradation machinery and possible evasion of host immune response journal May 2021
Feed in summer, rest in winter: microbial carbon utilization in forest topsoil journal September 2017
Metatranscriptomic Study of Common and Host-Specific Patterns of Gene Expression between Pines and Their Symbiotic Ectomycorrhizal Fungi in the Genus Suillus journal October 2016
Metatranscriptomics Reveals the Diversity of Genes Expressed by Eukaryotes in Forest Soils journal January 2012
Leaf and Root-Associated Fungal Assemblages Do Not Follow Similar Elevational Diversity Patterns journal June 2014
Welcome to the Tidyverse journal November 2019
Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems journal January 2006
Nitrogen Mineralization Following Fertilization of Douglas‐fir Forests with Urea in Western Washington journal September 2004
The Niche Exploitation Pattern of the Blue-Gray Gnatcatcher journal February 1967
Strong primer bias for Tulasnellaceae fungi in metabarcoding: Specific primers improve the characterization of the mycorrhizal communities of epiphytic orchids journal November 2021

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