ABSTRACT

In the nutrient poor soils of boreal forests, root-associated fungal communities are key determinants of ecosystem structure and stability. These communities are sensitive to anthropogenic nitrogen deposition and climate change, with alterations in their composition and function having global consequences for soil carbon storage and release. Our high temporal resolution metatranscriptomic analysis of Norway spruce fine roots and their associated fungal communities from nutrient limited and nutrient enriched forest soils revealed changes in host tree processes that resulted in alterations in the taxonomic composition and biological functions of the belowground fungal community. Specifically, in response to nutrient enrichment host trees reduced expression of sugar transporters and increased defence responses, causing the tree-microbe relationship to rebalance from friend towards foe. This altered interaction resulted in decreased coordination of microbial and tree functions related to growth, nutrient transport, and pre-symbiotic molecular signalling. Increased soil nutrient availability benefited versatile melanotic Ascomycetes (Cenococcum geophilum and Meliniomyces species) at the expense of Basidiomycetes with lignin-degrading capabilities (Piloderma and Cortinarius species), shifting the carbon balance of boreal soils towards greater accumulation of recalcitrant fungal necromass and lower rates of soil carbon turnover. This response to increased nutrient availability is in accord with evidence showing that trees exposed to elevated CO2 increased belowground carbon allocation, likely resulting from progressive nutrient limitation. Unravelling the contrasting impacts elevated CO2 and increased nutrient availability have on biodiversity and soil carbon sequestration is crucial for efforts to anticipate changes in future ecosystem function and stability. The metatranscriptomic approach utilised here provides previously lacking functional insight into active biological responses and structural changes within fungal communities, which will be a powerful tool for informing strategic responses to environmental challenges in future climate conditions.

PROJECT FEATURES

  • Tools

    Three online tools are available to explore the data. Click here

  • ENA ACCESION NUMBERS

    Click here to obtain the ENA accession numbers for the samples.

  • Github repository

    Scripts, pipelines and code used in this project can be found here

  • Reports

    Access the reports for the analysis here

TOOLS

NORWAY SPRUCE FINE ROOTS

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Temporally resolved transcriptomic analysis of Norway spruce (Picea abies) fine roots grown in nutrient-deficient and nutrient-enriched forest plots in the boreal region of Northern Sweden.

ROOT-ASSOCIATED FUNGAL COMMUNITY

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Temporally resolved metatranscriptomic analysis of the fungal community associated with the fine roots of Norway spruce, grown in nutrient-deficient and nutrient-enriched forest plots in the boreal region of Northern Sweden.

SYMBIOTIC COORDINATION

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Network analysis of the coordination between the host tree and the three most abundant root-associated fungi.

About the experimental site

Samples were collected at the Flakaliden research site (64°07′N, 19°27′E, altitude 310–320 m) in the boreal forests of northern Sweden (for details of the site, please refer to Haas et al., 2018). Boreal forests girdle the terrestrial environments of the northern latitudes, are dominated by coniferous tree species, and comprise the second largest biome in the world. Consequently, they play pivotal roles as wildlife habitats, sites of vast carbon sequestration, and the foundation of many important timber industries across the Northern Hemisphere. These soils are highly nutrient limited, as low annual soil temperatures hinder nutrient mineralisation rates and their isolation has shielded them from extensive anthropogenic nutrient deposition. A high-resolution map of the Flakaliden research site is provided in Extended Data Figure 1A. Treatment with a balanced nutrient solution of designated experimental plots within the forest stand commenced in 1987. This treatment had a profound effect on tree growth, with trees from fertilized plots on average 4 m taller and with four times the above-ground biomass of trees grown on NL plots (Sigurdsson et al., 2013; Extended Data Figure 1H). Belowground biomass was also greater in trees from fertilized plots but to a lesser extent (Majdi and Andersson, 2005) and the percentage of root tips colonised by ectomycorrhizal fungi was significantly lower than in low-nutrient grown roots (Leppälammi-Kujansuu et al., 2013).

Extended Data Figure 1. Climatic and phenological metadata for the Flakaliden research site (64°07′N, 19°27′E, altitude 310–320 m). (A) Location and layout of the Flakaliden research site. (B) Air and soil temperature (soil temperatures recorded at Svartberget field research station (64°14′N, 19°34′E), in 2011), and precipitation recorded at Flakaliden in 2011. (C) Radiation and relative humidity recorded at Flakaliden in 2011. (D) Day length at Flakaliden in 2011. (E) Phenological milestones of Norway spruce grown at Flakaliden. (F) Cumulative length production and mortality of spruce roots (mm tube-1) in the mineral soil layer at Flakaliden. A green line indicates nutrient limited soil; a gold line indicates nutrient enriched soil. Modified from Majdi and Andersson, 2005. (G) Soil CO2 efflux (gCO2- cm-2 h-1) at Flakaliden. A green line indicates nutrient limited soil; a gold line indicates nutrient enriched soil. Modified from Olsson et al., 2005. (H) Tree height (m), aboveground biomass (kg tree-1) and belowground biomass (g m-2) of nutrient limited and nutrient enriched Norway spruce (Sigurdsson et al. 2013; Majdi and Andersson, 2005).

AUTHORS

Simon Law

I am a Researcher working at the Department of Forest Genetics and Plant Physiology, SLU. I obtained my PhD from the University of Western Australia and have been working at the Umeå Plant Science Centre for the past 4 years. Currently, I am using molecular techniques to describe the impact of seasonality and soil nutrient alteration on the ectomycorrhizal association between Norway spruce and fungal communities of the northern boreal forests of Sweden.

Alonso Serrano

Biologist and computer engineer working as bioinformatician at the Department of Forest Genetics and Plant Physiology, SLU. My goal is to apply machine learning to biology and to develop tools that help scientists get faster and reliable experimental results.

ANDREAS SCHNEIDER

I am a PhD student at the Umeå Plant Science Centre. I am studying fungi and bacteria in the Swedish forest, and how these microbial lifeforms are influenced by factors such as nitrogen addition and modern forestry practices. Targeted field experiments in combination with sequencing and chemical analysis methods allow us to assess these microbial communities under different conditions. As we learn more about microbial communities and the role they play in the forest, it will enable us to involve microbial life forms into planning of more efficient and sustainable forestry practices.

ZSOFIA RÉKA STANGL

I’m a plant physiologist and ecophysiologist. I work as a postdoc at the Dept. of Forest Ecology and Management (SLU) and I defended my PhD in 2017 at Umeå University. Currently I’m working on characterising the diurnal and seasonal dynamics of mesophyll conductance and the balance between the carbon and water cycle in various boreal tree species, using mostly stable isotope techniques. During the PhD I was working on plant acclimation to different growth temperatures in combination with low nitrogen availability or elevated CO2.

DAVID CASTRO

I’m an ecologist interested in how plants interact with their environment. During my master, I studied how plants change their biochemistry and physiology in response to drought stress. Currently, I’m doing my PhD, applying molecular biology to study the response of seedlings to fertilization and the impact of the fertilization on the plant-microbiome interactions.

MANFRED GRABHERR

BIO

JOHN SUNDH

My expertise is in the field of metagenomics. I develop and run workflows and tools to study microbial populations.

TORGNY NäSHOLM

BIO

NATHANIEL STREET

I have a passion for trees and am interested in how phenotypic variation among individuals is determined by genome variation. My research focuses heavily on gene expression variation and the use of high throughput sequencing methods. This has led us to dedicating time to web resource development to offer access to the data resources developed and, most recently, to exploring the fascinating relationships between trees and their associated microbiomes.

VAUGHAN HURRY

BIO

REFERENCES

Sigurdsson, B. D., Medhurst, J. L., Wallin, G., Eggertsson, O. & Linder, S. Growth of mature boreal Norway spruce was not affected by elevated [CO2] and/or air temperature unless nutrient availability was improved. Tree Physiol 33, 1192-1205, doi:10.1093/treephys/tpt043 (2013).