skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Long‐term nitrogen fertilization inhibits carbon and nitrogen loss during late‐stage fungal necromass decomposition depending on necromass chemistry
Abstract Fungal necromass is increasingly recognized as a key component of soil carbon (C) and nitrogen (N) cycling. However, how C and N loss from fungal necromass during decomposition is impacted by global change factors such as anthropogenic N addition and changes to soil C supply (e.g. via changing root exudation and rhizosphere priming) remains unclear and understudied relative to plant tissues.To address these gaps, we conducted a year‐long decomposition experiment with four species of fungal necromass incubated across four forested sites in plots that had received inorganic N and/or labile C fertilization for two decades in Minnesota, USA.We found that necromass chemistry was the primary driver of C and N loss from fungal necromass as well as the response to fertilization. Specifically, N addition suppressed late‐stage decomposition, but this effect was weaker in melanin‐rich necromass, contrary to the hypothesis based on plant litter dynamics that N addition should suppress the decomposition of more complex organic molecules. Labile C addition had no effect on either the early or late stages of necromass decomposition.Nitrogen release from necromass also varied among species, with N‐poor necromass having lower N release after controlling for differences in mass loss via regression. The relatively minor effects of N fertilization on the proportion of initial necromass N released suggest that N demand by decomposers is the primary control on N loss during fungal necromass decomposition.Synthesis. Together, our results stress the importance of the afterlife effects of fungal chemical composition to forest soil C and N cycles. Further, they demonstrate that C and N release from this critical pool can be reduced by ongoing anthropogenic N addition.  more » « less
Award ID(s):
1831944
PAR ID:
10659483
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
John Wiley & Sons, Ltd
Date Published:
Journal Name:
Journal of Ecology
Volume:
113
Issue:
9
ISSN:
0022-0477
Page Range / eLocation ID:
2401 to 2413
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Wolfe, Benjamin E (Ed.)
    ABSTRACT Microbial necromass contributes significantly to both soil carbon (C) persistence and ecosystem nitrogen (N) availability, but quantitative estimates of C and N movement from necromass into soils and decomposer communities are lacking. Additionally, while melanin is known to slow fungal necromass decomposition, how it influences microbial C and N acquisition as well as elemental release into soils remains unclear. Here, we tracked decomposition of isotopically labeled low and high melanin fungal necromass and measured13C and15N accumulation in surrounding soils and microbial communities over 77 d in a temperate forest in Minnesota, USA. Mass loss was significantly higher from low melanin necromass, corresponding with greater13C and15N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in13C and/or15N at all sampling points, with enrichment being consistently higher on low melanin necromass and earlier in decomposition. Similar patterns of preferential C and N enrichment of many bacterial and fungal genera early in decomposition suggest that both microbial groups co-contribute to the rapid assimilation of resource-rich soil organic matter inputs. While overall richness of taxa enriched in C was higher than in N for both bacteria and fungi, there was a significant positive relationship between C and N in co-enriched taxa. Collectively, our results demonstrate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate but also necromass C and N release and that both elements are rapidly co-utilized by diverse bacterial and fungal decomposers in natural settings. IMPORTANCERecent studies indicate that microbial dead cells, particularly those of fungi, play an important role in long-term carbon persistence in soils. Despite this growing recognition, how the resources within dead fungal cells (also known as fungal necromass) move into decomposer communities and soils are poorly quantified, particularly in studies based in natural environments. In this study, we found that the contribution of fungal necromass to soil carbon and nitrogen availability was slowed by the amount of melanin present in fungal cell walls. Further, despite the overall rapid acquisition of carbon and nitrogen from necromass by a diverse range of both bacteria and fungi, melanization also slowed microbial uptake of both elements. Collectively, our results indicate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate, but also necromass carbon and nitrogen release into soil as well as microbial resource acquisition. 
    more » « less
  2. Nikel, Pablo Ivan (Ed.)
    ABSTRACT Bacteria are major drivers of organic matter decomposition and play crucial roles in global nutrient cycling. Although the degradation of dead fungal biomass (necromass) is increasingly recognized as an important contributor to soil carbon (C) and nitrogen (N) cycling, the genes and metabolic pathways involved in necromass degradation are less characterized. In particular, how bacteria degrade necromass containing different quantities of melanin, which largely control rates of necromass decompositionin situ, is largely unknown. To address this gap, we conducted a multi-timepoint transcriptomic analysis using three Gram-negative, bacterial species grown on low or high melanin necromass ofHyaloscypha bicolor. The bacterial species,Cellvibrio japonicus, Chitinophaga pinensis, andSerratia marcescens, belong to genera known to degrade necromassin situ. We found that while bacterial growth was consistently higher on low than high melanin necromass, the CAZyme-encoding gene expression response of the three species was similar between the two necromass types. Interestingly, this trend was not shared for genes encoding nitrogen utilization, which varied inC. pinensisandS. marcescensduring growth on high vs low melanin necromass. Additionally, this study tested the metabolic capabilities of these bacterial species to grow on a diversity of C and N sources and found that the three bacteria have substantially different utilization patterns. Collectively, our data suggest that as necromass changes chemically over the course of degradation, certain bacterial species are favored based on their differential metabolic capacities.IMPORTANCEFungal necromass is a major component of the carbon (C) in soils as well as an important source of nitrogen (N) for plant and microbial growth. Bacteria associated with necromass represent a distinct subset of the soil microbiome and characterizing their functional capacities is the critical next step toward understanding how they influence necromass turnover. This is particularly important for necromass varying in melanin content, which has been observed to control the rate of necromass decomposition across a variety of ecosystems. Here we assessed the gene expression of three necromass-degrading bacteria grown on low or high melanin necromass and characterized their metabolic capacities to grow on different C and N substrates. These transcriptomic and metabolic studies provide the first steps toward assessing the physiological relevance of up-regulated CAZyme-encoding genes in necromass decomposition and provide foundational data for generating a predictive model of the molecular mechanisms underpinning necromass decomposition by soil bacteria. 
    more » « less
  3. Summary Anthropogenic nitrogen (N) deposition can alleviate N limitation and stimulate plant growth in many terrestrial ecosystems. While theoretical models often emphasize phosphorus limitations as a constraint on this positive N effect, the impact of N‐induced magnesium (Mg) and calcium (Ca) deficits due to soil acidification has been largely overlooked.Here, we synthesized data from 243 experiments across diverse terrestrial ecosystems to investigate the role of Mg and Ca in plant biomass responses to N addition.We found that the effect of N addition on aboveground biomass (AGB) shifted from neutral in low pH (≤ 4.5) to positive in medium (4.5–7.5) and high pH (> 7.5) soils. By contrast, belowground biomass (BGB) responses to N addition were independent of soil pH, leading to asymmetric increases in AGB and BGB. These variations in biomass accumulation across pH levels were primarily explained by changes in foliar Mg and Ca concentrations, which were negatively affected by N addition in low‐pH soils but remained stable in medium and high‐pH soils.Our findings underscore the critical role of Mg and Ca in modulating plant responses to N fertilization, providing new insights for improving Earth system models and better predicting climate–biosphere feedback. 
    more » « less
  4. Summary Unlike most ectomycorrhizal (EM) fungi,Cenococcum geophilumis a prolific producer of sclerotia, which represent a large and persistent, yet rarely quantified pool of EM fungal biomass and carbon in soils. How biomass of these asexual propagules is impacted by global change factors, such as anthropogenic nitrogen (N) deposition, remains unquantified.This study examined the effects of long‐term experimental N fertilization on the standing biomass, abundance, and size ofC. geophilumsclerotia in an oak (Quercusspp.) savanna ecosystem at Cedar Creek Ecosystem Science Reserve in Minnesota, USA.Standing sclerotia biomass in the control treatment averaged 192 g m−2(95% CI = 136–267 g m−2) and declined sharply under N enrichment, by 44% (95% CI = −53–79%) and 66% (95% CI = 39–82%) in the low N (5.4 g N m−2 yr−1) and high N (17 g N m−2 yr−1) treatments, respectively. Sclerotia abundance also declined under both fertilization levels by 58% (95% CI: 8–81%) and 62% (95% CI: 12–84%), while sclerotia diameter was significantly reduced only under high N.Given their high carbon content, melanization, and long persistence, the observed declines inC. geophilumsclerotia (c.84–127 g m−2) represent substantial losses from belowground carbon (C) pools. These findings indicate that chronic N deposition suppresses the formation of a functionally important and recalcitrant fungal structure, likely impacting soil C storage and mycorrhizal functional diversity. 
    more » « less
  5. ABSTRACT Mycelial residues, also known as fungal necromass, represent a substantial fraction of soil organic matter (SOM) pools in terrestrial ecosystems worldwide. Although microbial decomposers are increasingly recognised as key drivers of fungal necromass carbon stock formation, the diversity and composition of their microbial predators—and the roles these predators play in mediating fungal necromass decomposition—have not been explored to date. To address this gap, we produced fungal necromass of varying biochemical quality fromHyaloscypha bicolorand decomposed it in forest topsoil in Minnesota, USA, to investigate how microbial decomposer (bacteria and fungi) and predator (protists and nematodes) communities differ between soil and necromass. We also examined whether microbial predators influence the abundance of fungal necromass decomposers and affect necromass decomposition rates. Over two sampling times (4 and 12 weeks), necromass exhibited rapid early mass loss followed by reduced decay, with a higher stabilised mass in high melanin necromass. Microbial abundances were higher in necromass than in surrounding soil, especially in low melanin necromass. Community composition of both decomposers and their predators differed between soil and necromass and shifted markedly with necromass quality and decomposition stage. Predator community composition was linked to bacterial and fungal abundances at both early and late stages of decay and was marginally associated with decomposition rates. We conclude that fungal necromass acts as a microbial ‘hotspot’ not only for decomposers but also for their predators. These findings highlight the importance of microbial predator–decomposer interactions to better understand the formation of fungal‐derived SOM. 
    more » « less