Figure 1a: Litter inputs join SOM as light POM, which is
largely composed of undecomposed litter fragments. As decomposition
progresses, litter-derived SOM can more easily become incorporated into
aggregates in heavy POM or microbial decomposition products and
necromass can preferentially sorb to soil mineral surfaces as MAOM.1b: Roots and root-associated fungal symbionts can enhance both
retention or loss of litter in light POM (top), heavy POM (middle), and
MAOM (bottom) pools.
Living roots and their associated fungi alter SOM formation by sending
C-rich exudates to the rhizosphere to enhance decomposition and acquire
N (Bais et al., 2006; Grayston et al., 1997). However, a high degree of
uncertainty remains in whether this increases or decreases soil C
accumulation. In Figure 1b, we diagram potential hypotheses for how
roots could alter litter loss from light POM and the accumulation of new
heavy POM and MAOM through distinct mechanisms. First, root stimulation
of microbial decomposition to mineralize soil N can increase the loss of
unprotected light POM through the rhizosphere priming effect (Cheng et
al., 2014). However, there is also evidence that roots and symbiotic
fungi can outcompete saprotrophic microbes for resources like water and
nutrients leading to the suppression of decomposition (Fernandez &
Kennedy, 2016). Second, as litter inputs are transferred into more
protected heavy POM, root ingrowth has the potential to both invade
aggregates and increase the formation rate of new aggregates (Six et
al., 2000). Finally, roots can enhance new MAOM formation by increasing
the efficiency of microbial litter decomposition, resulting in greater
microbial biomass production and the formation of microbial necromass
(Liang et al., 2017). This necromass can associate with mineral surfaces
and is the main precursor to MAOM in grassland ecosystems (Angst et al.,
2021). However, roots may also deplete new, litter-derived MAOM as
recent evidence suggests that roots can actively mine MAOM for nutrients
(Jilling et al., 2021) and that root exudate compounds can displace MAOM
from soil minerals (Keiluweit et al., 2015). As such, predicting whether
roots will drive a net gain or loss of soil C is hindered by uncertainty
in how roots impact SOM formation in these different pools.
The extent to which roots and mycorrhizal fungi facilitate SOM formation
or loss in agricultural ecosystems may be modulated by fertilization.
For example, some N-limited plants can dynamically shift C allocation
belowground to root exudation and mycorrhizal symbionts to stimulate
microbial decomposition in the rhizosphere and increase N acquisition
(Brzostek et al., 2014; Kane et al., 2022). When N limitation is
alleviated by fertilization, plants can also reduce belowground C
allocation, suppressing SOM decomposition (Eastman et al., 2021; Frey et
al., 2014). The degree to which fertilization alters SOM cycling also
depends upon the activity of saprotrophic soil microbial decomposers. In
contrast to plants, soil microbes are primarily understood to be energy,
or carbon, limited (Soong et al., 2020). As such, organic fertilizer
that contains C and N can prime microbial activity and decomposition
relative to inorganic N fertilizer (Cui et al., 2022; Ndung’u et al.,
2021). However, uncertainty remains in the extent to which the priming
of microbial activity leads to net soil C losses by enhancing
decomposition or net C gains by promoting the production of microbial
necromass that can form MAOM. Collectively, the effect of fertilization
on SOM formation depends upon the strength of plant-microbe interactions
and the form of fertilizer applied, but the magnitude of this effect is
uncertain.
Given the uncertainty above, our objectives were to: 1)
determine how living roots and symbiotic fungi influence litter
decomposition and SOM formation in distinct SOM pools and 2) assess how
microbially-driven SOM formation is altered by fertilization. For the
first objective, we assayed the net effect of the opposing hypotheses
illustrated in Figure 1. For the second objective, we tested two
hypotheses: (1) the effect of living roots on SOM formation would be
strongest in unfertilized soil and (2) organic fertilizer would
accelerate microbial decomposition and SOM cycling to a greater extent
than inorganic fertilizer (SI Figure 1 ). To meet our
objectives, we measured the effects of living roots and fungi on new SOM
formation from isotopically enriched litter over one growing season. We
incubated litter inputs in soil cores that were open to roots and fungal
ingrowth (root), that excluded roots but were open to fungal ingrowth
(fungal), or that excluded both roots and fungi (none) to quantify the
effect of living roots and fungi on new SOM formation (SI Fig.2 ). We installed ingrowth cores in Miscanthus x
giganteus (herein miscanthus) plots with different nutrient treatments
to investigate the effect of soil N and C availability on how roots,
mycorrhizal fungi, and saprotrophic microbes drive the transfer of
litter C and N into light POM, heavy POM, and MAOM. We used the
bioenergy feedstock crop miscanthus as a study system because it
produces extensive root systems to overcome nutrient limitation
(Dohleman & Long, 2009; Heaton et al., 2008) and because miscanthus
agriculture typically increases SOM levels (Harris et al., 2015).
Further, because bioenergy offers the potential to become a C neutral or
C negative alternative to fossil fuels, it is particularly critical to
investigate what drives SOM accumulation in these ecosystems (Hanssen et
al., 2020).
We show that miscanthus roots increased litter decomposition but did not
lead to a net C loss because roots enhanced the incorporation of litter
C into heavy POM. Roots also selectively mobilized litter N from both
POM pools. As such, roots can transfer C into a more persistent SOM pool
while still enhancing N mining. These root effects did not depend on
fertilization. However, organic fertilization enhanced microbial litter
decomposition without increasing litter incorporation in MAOM.