Introduction:
Managing soils in agricultural systems to sequester carbon (C) in soil
organic matter (SOM) may be a powerful approach to offset anthropogenic
C emissions (Lal, 2004). Soils are the largest terrestrial C pool, and
experimental manipulations like changing vegetation type, increasing
organic inputs, or altering management practices demonstrate the
potential for significant and rapid SOM accumulation (Minasny et al.,
2017; Paustian et al., 2016). However, there is a high degree of
uncertainty in understanding, predicting, and optimizing soil C
accumulation (Sulman et al., 2018). Much of this uncertainty arises
because plant roots and soil microbes, the active drivers of soil
biogeochemical cycling, both destabilize and stabilize SOM through
simultaneously occurring processes. As such, our ability to optimize
soil C sequestration relies on improving our understanding of how roots
and microbes drive the transfer of new litter C inputs into SOM.
As per the current understanding of SOM formation, litter inputs are
decomposed into simpler compounds that can be physically protected from
microbial decomposers by occlusion in soil aggregates or sorption to
mineral surfaces (Lehmann & Kleber, 2015). As such, SOM is often
delineated into three main pools: undecomposed or partially-decomposed
particulate organic matter (here, light POM), aggregate-occluded SOM
(here, heavy POM), and mineral associated organic matter (MAOM)
(Lavallee et al., 2020). Light POM accumulation depends upon the balance
between litter inputs to soil and litter decomposition, and can
accumulate with no apparent upper limit but is also vulnerable to
factors like warming that enhance decomposition rates (Benbi et al.,
2014; Cotrufo et al., 2019). Heavy POM is operationally separated from
light POM by density fractionation and is linked with stable soil
aggregates (Lavallee et al., 2020). Accumulation in this pool may
saturate and is vulnerable to factors like soil disturbance and land use
change (Bronick & Lal, 2005). MAOM is generally considered to be the
most stable or protected form of SOM (Cotrufo et al., 2013; Liang et
al., 2017). However, MAOM saturates such that accumulation may only be
feasible in ecosystems with a current deficit, like degraded
agricultural soils (Stockmann et al., 2015). To optimize soil C
sequestration in managed ecosystems, understanding what drives the
transfer of new litter inputs between these SOM pools is important for
enhancing our predictive understanding of how much soil C can accumulate
and how persistent this soil C may be in a changing climate.
Living roots and their associated fungi alter the formation and
stabilization of SOM 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
leads to net gains or losses in soil C. In Figure 1, we diagram
potential hypotheses for how roots could stabilize or destabilize SOM in
the light POM, heavy POM, and MAOM pools through distinct mechanisms.
First, root stimulation of microbial decomposition to mineralize soil N
can lead to a 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 alter this stabilization by both invading aggregates and
increasing the formation rate of new aggregates (Six et al., 2000).
Finally, roots can enhance stable MAOM formation by increasing the
efficiency of microbial litter decomposition, resulting in greater
microbial biomass production and the formation of microbial necromass.
This necromass can associate with mineral surfaces and is the main
precursor to MAOM in grassland ecosystems (Angst et al., 2021; Liang et
al., 2017). However, roots may also destabilize 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 stabilization in these
different pools.