Distinct carbon fractions drive a generalisable two‐pool model of fungal necromass decomposition

Abstract

Fungi represent a rapidly cycling pool of carbon (C) and nitrogen (N) in soils. Understanding of how this pool impacts soil nutrient availability and organic matter fluxes is hindered by uncertainty regarding the dynamics and drivers of fungal necromass decomposition. Here we assessed the generality of common models for predicting mass loss during fungal necromass decomposition and linked the resulting parameters to necromass substrate chemistry. We decomposed 28 different types of fungal necromass in laboratory microcosms over a 90‐day period, measuring mass loss on all types, and N release on a subset of types. We characterised the initial chemistry of each necromass type using: (a) fibre analysis methods commonly used for plant tissues, (b) initial melanin and nitrogen (N) concentrations and (c) Fourier transform infrared (FTIR) spectroscopy to assess the presence of bonds associated with common biomolecules. We found universal support for an asymptotic model of decomposition, which assumes that fungal necromass consists of an exponentially decomposing ‘fast’ pool, and a ‘slow’ pool that decomposes at a rate approaching zero. The strongest predictor of the fast pool decay rate (k) was the proportion of cell soluble components, though initial N concentration also predicted k, albeit more weakly. The size of the slow pool was best predicted by the acid non‐hydrolysable fraction, which was positively correlated with melanin‐associated aromatics. Nitrogen dynamics varied by necromass type, ranging from net N release to net immobilisation. The maximum quantity of N immobilised was inversely related to cell soluble contents and k, as positively related to FTIR spectra associated with cell wall polysaccharides. Collectively, our results indicate that the decomposition of fungal necromass in soils can be described as having two distinct stages that are driven by different components of substrate C chemistry, with implications for rates of N availability and organic matter accumulation in soils. A free Plain Language Summary can be found within the Supporting Information of this article.

Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization

“…When fungal cells lyse, soluble components within the cell such as amino acids and sugars become available to the surrounding environment and can sorb to mineral surfaces or be consumed by decomposers for further transformation (see below). Depolymerization of beta‐glucans and chitin, the dominant components of fungal cell walls, occurs over the course of days to weeks (See et al, 2020), providing opportunities for sorption of amino sugar monomers or polysaccharide chains (Keiluweit et al, 2012). As hyphal necromass decomposition proceeds, more slowly decomposing cell wall components yield more complex molecules for organo‐mineral interactions.…”

“…Fungal necromass contains a higher proportion of labile C (e.g., cell soluble sugars, polysaccharide chains) than root litter, and decomposition rates of labile components of hyphae are commonly measured in days, while fine root decomposition is commonly measured over the course of years (See et al, 2019, 2020). As hyphal necromass decomposes, it forms the base of a complex food web of microbial decomposers dominated by bacteria (López‐Mondéjar et al, 2018) that anchor themselves to the hyphal remnants and adjacent mineral surfaces with EPS (Figure 2c).…”

Tree biomass allocation differs by mycorrhizal association

“…This pattern is particularly strong in coniferous forests and nutrient‐limited systems, where there is a trade‐off in allocation of C to mycorrhizae rather than roots, likely as a strategy to liberate organic forms of soil nutrients (Ouimette et al, 2019; Vicca et al, 2012). Further, an emerging understanding of the stability and long‐term persistence of fungal versus root‐derived soil carbon suggests that fungal necromass is comprised of a higher proportion of fast‐decaying carbon compared with root necromass (See et al, 2021), which should contribute more to the mineral‐associated organic matter pool (Lavallee et al, 2019), resulting in long‐term soil C storage (Lugato et al, 2021). However, recent studies demonstrate larger pools of mineral‐bound C in AM systems (Cotrufo et al, 2019; Craig et al, 2018), indicating that the higher C allocation to fungal tissues in ECM systems does not entirely offset belowground C inputs leading to stable soil C pools in AM‐dominated ecosystems.…”

Soil organic carbon fractionation and metagenomics pipeline to link carbon content and stability with microbial composition – First results investigating fungal endophytes

“…The fungal isolate 1852 increased the chemical recalcitrance of carbon in the AggC fraction. It is a dark pigmented fungus that likely has melanin present in the fungal cell wall that can remain in the soil for longer than necromass from non-melanised fungi (Fernandez et al, 2016; Fernandez and Kennedy, 2018; See et al, 2021). Melanin content in soil has been correlated with higher total soil C content (Siletti et al, 2017).…”