Introduction
Soil organic matter (SOM) is known to be the largest C pool in
terrestrial ecosystems, ranging from 1500 to 2000 Pg in the top meter.
This equals two to three times the amount of C stored in the vegetation,
which is approximately 500 Pg (Amundson, 2001; Butler & Day, 1998;
Dixon et al., 1994). Among the various sources of SOM in forest
ecosystems, dead mycelia are probably among the largest ones. It has
been suggested that the majority of C stored in the deeper horizons of
boreal forest soils originates from the allocation of photosynthate to
ectomycorrhizal fungi (Clemmensen et al., 2013). The annual allocation
of carbon into mycorrhizal fungi can constitute up to 22% of the annual
net primary productivity (Hobbie & Hobbie, 2006). This major
contribution suggests the profound importance of these fungi in the
overall allocation of carbon in both litter and soil compartments.
Estimates of ectomycorrhizal (EM) biomass, which constitutes the major
fraction of soil fungal biomass, typically range from 100 to 600 kg
ha-1 (Hendricks, Mitchell, Kuehn, & Pecot, 2016;
Wallander, Göransson, & Rosengren, 2004) and, together with roots,
produces more than 50% of the dissolved organic carbon in forest’s soil
(Högberg & Högberg, 2002). Significant amounts of mycelia are produced
in soil layers below the depth of 10 cm (Boström, Comstedt, & Ekblad,
2007) and in the litter, where the dry fungal biomass per g substrate
can be more than 10-fold that of soil (Baldrian et al., 2013). In forest
soil and litter, which are often N limited, fungal mycelia are more
attractive than plant residues as a target for decomposers, given their
high content of N, which can be 3 up to 30 times greater than in plant
litter (Koide & Malcolm, 2009; Mouginot et al., 2014). Due to the large
fluxes of C and nutrients into the soil through fungal necromass, a
better understanding of the decomposition dynamics of fresh fungal
litter may improve our understanding of SOM dynamics, and how these two
are related.
A major driving factor of litter decomposition is the initial litter
“quality”, i.e. litter chemical composition (Berg, 1984). In general,
decomposition is favoured by relatively low litter C:N ratios (Cleveland
& Liptzin, 2007), which might help to maintain the low C:N ratio of
microbial cells (Manzoni, Trofymow, Jackson, & Porporato, 2010). Yet,
there is increasing evidence that other aspects of chemical litter
quality beyond basic stoichiometry also affect decomposition rates
(Wilkinson, Alexander, & Johnson, 2011).
To date, the number of observations about the decomposition rates of EM
fungi is limited, as well as our knowledge on their main drivers. It has
been hypothesised that EM fungal necromass decomposition is driven
mainly by its necromass “quality”, which, similarly to plant litter,
refers to fungal necromass chemistry and morphology. Previous research
found a significant positive relationship between the N concentration in
the fungal tissues and its decomposition (Christopher W Fernandez &
Koide, 2014; Koide & Malcolm, 2009).
The chemical composition of ectomycorrhizal fungal mycelium varies
widely among fungal species and possibly contributes to the variation in
decomposition rates of EM fungal necromass. While the cytoplasmic
fraction does not likely play a significant role in the decomposition of
EM necromass due to its high lability (Drigo, Anderson, Kannangara,
Cairney, & Johnson, 2012), it seems that the composition of the cell
wall cell cel fraction drives the long-term decomposition of EM
extramatrical necromass. The chemical composition of the cell wall of EM
fungi varies with age, genotype, taxon, and environment (Bowman & Free,
2006; Feofilova, 2010). EM fungal cell walls are composed mainly by
polysaccharides such as glucans and chitin (70-90% of dry biomass),
proteins, which contains from 40 to 60% of cell wall total N, and
melanins. The latter, despite being a minor component and highly
variable in concentration across different taxa (Butler & Day, 1998a),
is linked to the tolerance of various environmental stressors
(Christopher W Fernandez & Koide, 2013; Rosas & Casadevall, 1997; Wang
& Casadevall, 1994).
During the last decades, several studies suggested that differences in
initial concentrations of the main classes of chemical fungal cell-wall
compounds (proteins, carbohydrates, melanin) underpin necromass
degradation (Christopher W Fernandez & Koide, 2012, 2014). Yet, there
are many uncertainties concerning the mechanisms behind this
relationship. These uncertainties range from the dynamics of secondary
compounds contents during the decomposition process to the actual
interaction between the components themselves. Moreover, we may not
assume that the initial concentration of cell-wall compounds (Berg,
2000; Melillo, Aber, & Muratore, 1982), is a dominant predictor of the
decomposition rate and dynamics. The fungal wall structure is highly
variable. In contrast to plant litter, the fungal cell wall retains
considerable plasticity despite the presence of a relatively rigid
scaffold formed by chitin fibrils and α-1,3-glucans. This plasticity
allows to easily reshape the molecular architecture of mycelia to
survive through different external stress. In addition, the fungal cell
walls contain an extensive covalent cross-linking of glucans and chitin
(Cairney, 2012; Kang et al., 2018). These dissimilarities suggest that
we might need to consider different drivers to predict its decomposition
compared to plants. So far, no previous research has explored the role
of the interaction between cell-wall components in the decomposition of
EM necromass. Nor did previous research consider the impacts of changes
in these cell wall components during decomposition. Since all these
components are highly interconnected and each one has a specific role in
maintaining the cell wall structure and function, an extensive temporal
analysis of dynamics of their composition through the fungal litter
degradation process will improve our understanding of the mechanisms
behind fungal necromass decomposition.
In this paper we examine the dynamics in the most abundant cell-wall
compounds (chitin, glucans and melanin) from EMF mycelia necromass
across 6 EM fungi species, seeking an answer to the question of whether
the dynamics in composition and concentration of these compounds is
linked to mycelium decomposition dynamics. Hereto we seek an answer to
three research questions: 1) Do the initial concentrations of the
cell-components alone predict fungal litter decomposition?; 2) Can the
concentration dynamics of chitin, glucans and melanin during the
decomposition process predict the dynamics of fungal litter mass loss?;
and 3) Do distinct EM fungal species exhibit a similar temporal dynamics
of losing cell wall components during the decomposition process?