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.