skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Friday, December 13 until 2:00 AM ET on Saturday, December 14 due to maintenance. We apologize for the inconvenience.


Title: Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition
Summary

Interactions between symbiotic ectomycorrhizal (EM) and free‐living saprotrophs can result in significant deceleration of leaf litter decomposition. While this phenomenon is widely cited, its generality remains unclear, as both the direction and magnitude of EM fungal effects on leaf litter decomposition have been shown to vary among studies.

Here we explicitly examine how contrasting leaf litter types and EM fungal communities may lead to differential effects on carbon (C) and nitrogen (N) cycling. Specifically, we measured the response of soil nutrient cycling, litter decay rates, litter chemistry and fungal community structure to the reduction of EM fungi (via trenching) with a reciprocal litter transplant experiment in adjacentPinus‐ orQuercus‐dominated sites.

We found clear evidence of EM fungal suppression of C and N cycling in thePinus‐dominated site, but no suppression in theQuercus‐dominated site. Additionally, in thePinus‐dominated site, only thePinuslitter decay rates were decelerated by EM fungi and were associated with decoupling of litter C and N cycling.

Our results support the hypothesis that EM fungi can decelerate C cycling via N competition, but strongly suggest that the ‘Gadgil effect’ is dependent on both substrate quality and EM fungal community composition. We argue that understanding tree host traits as well as EM fungal functional diversity is critical to a more mechanistic understanding of how EM fungi mediate forest soil biogeochemical cycling.

 
more » « less
PAR ID:
10455671
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
226
Issue:
2
ISSN:
0028-646X
Page Range / eLocation ID:
p. 569-582
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    The extent to which ectomycorrhizal (ECM) fungi decay soil organic matter (SOM) has implications for accurately predicting forest ecosystem response to climate change. Investigating the distribution of gene traits associated with SOM decay among ectomycorrhizal fungal communities could improve understanding of SOM dynamics and plant nutrition. We hypothesized that soil inorganic nitrogen (N) availability structures the distribution of ECM fungal genes associated with SOM decay and, specifically, that ECM fungal communities occurring in inorganic N‐poor soils have greater SOM decay potential.

    To test this hypothesis, we paired amplicon and shotgun metagenomic sequencing of 60 ECM fungal communities associating withQuercus rubraalong a natural soil inorganic N gradient.

    Ectomycorrhizal fungal communities occurring in low inorganic N soils were enriched in gene families involved in the decay of lignin, cellulose, and chitin. Ectomycorrhizal fungal community composition was the strongest driver of shifts in metagenomic estimates of fungal decay potential. Our study simultaneously illuminates the identity of key ECM fungal taxa and gene families potentially involved in the decay of SOM, and we link rhizomorphic and medium‐distance hyphal morphologies with enhanced SOM decay potential.

    Coupled shifts in ECM fungal community composition and community‐level decay gene frequencies are consistent with outcomes of trait‐mediated community assembly processes.

     
    more » « less
  2. Abstract

    Litter decomposition is a key ecological process that determines carbon (C) and nutrient cycling in terrestrial ecosystems. The initial concentrations of C and nutrients in litter play a critical role in this process, yet the global patterns of litter initial concentrations of C, nitrogen (N) and phosphorus (P) are poorly understood.

    We employed machine learning with a global database to quantitatively assess the global patterns and drivers of leaf litter initial C, N and P concentrations, as well as their returning amounts (i.e. amounts returned to soils).

    The medians of litter C, N and P concentrations were 46.7, 1.1, and 0.1%, respectively, and the medians of litter C, N and P returning amounts were 1.436, 0.038 and 0.004 Mg ha−1 year−1, respectively. Soil and climate emerged as the key predictors of leaf litter C, N and P concentrations. Predicted global maps showed that leaf litter N and P concentrations decreased with latitude, while C concentration exhibited an opposite pattern. Additionally, the returning amounts of leaf litter C, N and P all declined from the equator to the poles in both hemispheres.

    Synthesis: Our results provide a quantitative assessment of the global concentrations and returning amounts of leaf litter C, N and P, which showed new light on the role of leaf litter in global C and nutrients cycling.

     
    more » « less
  3. Abstract

    Decomposition is a major component of global carbon cycling. However, approximately 50% of wood necromass and a small proportion of leaf litter do not contact the forest floor, and the factors that regulate the decomposition above the forest floor are largely untested. We hypothesized that separation from soil resources causes slower decomposition rates above the forest floor. Specifically, we tested whether slower decomposition results from decreased nutrient availability (the nutrient limitation hypothesis) and/or microbial dispersal limitation (the dispersal limitation hypothesis) in the absence of soil resources.

    We tested these hypotheses by combining experimental manipulations of epiphytes and macronutrient fertilization with elemental analyses and community metabarcoding (fungi and prokaryotes). Specifically, we compared wood stick and cellulose decomposition among three treatments: an unaltered trunk section, an epiphyte mat, and a ‘removal treatment’ where an epiphyte mat was removed to test the effect of soil resources. We also performed a factorial fertilization experiment to test the effects of nitrogen (N) and phosphorus (P) on the decomposition of suspended cellulose.

    Decomposition rates were fastest on the epiphyte mats, intermediate in the removal treatment and slowest in the controls. Phosphorus addition increased decomposition rates in the fertilization experiment, and greater P concentrations, along with some micronutrients, were associated with increased rates of decomposition on the epiphyte mats and in the removal treatments. Locally dispersed fungi dominated the wood stick communities, indicating that fungal dispersal is limited in the canopy, and fungal saprotrophs were associated with increased rates of decomposition on the epiphytes.

    These experiments show that slowed decomposition above the forest floor is caused, in part, by separation from soil resources. Moreover, our findings provide support for both the nutrient limitation and dispersal limitation hypotheses and indicate that mechanisms regulating canopy‐level decomposition differ from those documented on the forest floor. This demonstrates the need for a holistic approach to decomposition that considers the vertical position of necromass as it decomposes. Further experimentation is necessary to quantify interactions between community assembly processes, nutrient availability, substrate traits, and microclimate.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  4. Summary

    Leaf decomposition varies widely across temperate forests, shaped by factors like litter quality, climate, soil properties, and decomposers, but forest heterogeneity may mask local tree influences on decomposition and litter‐associated microbiomes. We used a 24‐yr‐old common garden forest to quantify local soil conditioning impacts on decomposition and litter microbiology.

    We introduced leaf litter bags from 10 tree species (5 arbuscular mycorrhizal; 5 ectomycorrhizal) to soil plots conditioned by all 10 species in a full‐factorial design. After 6 months, we assessed litter mass loss, C/N content, and bacterial and fungal composition. We hypothesized that (1) decomposition and litter‐associated microbiome composition would be primarily shaped by the mycorrhizal type oflitter‐producing trees, but (2) modified significantly by underlying soil, based on mycorrhizal type of theconditioning trees.

    Decomposition and, to a lesser extent, litter‐associated microbiome composition, were primarily influenced by the mycorrhizal type of litter‐producing trees. Interestingly, however, underlying soils had a significant secondary influence, driven mainly by tree species, not mycorrhizal type. This secondary influence was strongest under trees from the Pinaceae.

    Temperate trees can locally influence underlying soil to alter decomposition and litter‐associated microbiology. Understanding the strength of this effect will help predict biogeochemical responses to forest compositional change.

     
    more » « less
  5. Summary

    Ecosystems with ectomycorrhizal plants have high soil carbon : nitrogen ratios, but it is not clear why. The Gadgil effect, where competition between ectomycorrhizal and saprotrophic fungi for nitrogen slows litter decomposition, may increase soil carbon. However, experimental evidence for the Gadgil effect is equivocal.

    Here, we apply resource‐ratio theory to assess whether interguild fungal competition for different forms of organic nitrogen can affect litter decomposition. We focus on variation in resource input ratios and fungal resource use traits, and evaluate our model's predictions by synthesizing prior experimental literature examining ectomycorrhizal effects on litter decomposition.

    In our model, resource input ratios determined whether ectomycorrhizal fungi suppressed saprotrophic fungi. Recalcitrant litter inputs favored the former over the latter, allowing the Gadgil effect only when such inputs predominated. Although ectomycorrhizal fungi did not always hamper litter decomposition, ectomycorrhizal nitrogen uptake always increased carbon : nitrogen ratios in litter.

    Our meta‐analysis of empirical studies supports our theoretical results: ectomycorrhizal fungi appear to slow decomposition of leaf litter only in forests where litter inputs are highly recalcitrant. We thus find that the specific contribution of the Gadgil effect to high soil carbon : nitrogen ratios in ectomycorrhizal ecosystems may be smaller than predicted previously.

     
    more » « less