skip to main content


Title: Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits
Abstract

Conceptual and empirical advances in soil biogeochemistry have challenged long-held assumptions about the role of soil micro-organisms in soil organic carbon (SOC) dynamics; yet, rigorous tests of emerging concepts remain sparse. Recent hypotheses suggest that microbial necromass production links plant inputs to SOC accumulation, with high-quality (i.e., rapidly decomposing) plant litter promoting microbial carbon use efficiency, growth, and turnover leading to more mineral stabilization of necromass. We test this hypothesis experimentally and with observations across six eastern US forests, using stable isotopes to measure microbial traits and SOC dynamics. Here we show, in both studies, that microbial growth, efficiency, and turnover are negatively (not positively) related to mineral-associated SOC. In the experiment, stimulation of microbial growth by high-quality litter enhances SOC decomposition, offsetting the positive effect of litter quality on SOC stabilization. We suggest that microbial necromass production is not the primary driver of SOC persistence in temperate forests. Factors such as microbial necromass origin, alternative SOC formation pathways, priming effects, and soil abiotic properties can strongly decouple microbial growth, efficiency, and turnover from mineral-associated SOC.

 
more » « less
Award ID(s):
1701652 1832210
NSF-PAR ID:
10363828
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Volume:
13
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Despite the large contribution of rangeland and pasture to global soil organic carbon (SOC) stocks, there is considerable uncertainty about the impact of large herbivore grazing onSOC, especially for understudied subtropical grazing lands. It is well known that root system inputs are the source of most grasslandSOC, but the impact of grazing on partitioning of carbon allocation to root tissue production compared to fine root exudation is unclear. Given that different forms of root C have differing implications forSOCsynthesis and decomposition, this represents a significant gap in knowledge. Root exudates should contribute toSOCprimarily after microbial assimilation, and thus promote microbial contributions toSOCbased on stabilization of microbial necromass, whereas root litter deposition contributes directly as plant‐derivedSOCfollowing microbial decomposition. Here, we used in situ isotope pulse‐chase methodology paired with plant and soil sampling to link plant carbon allocation patterns withSOCpools in replicated long‐term grazing exclosures in subtropical pasture in Florida,USA. We quantified allocation of carbon to root tissue and measured root exudation across grazed and ungrazed plots and quantified lignin phenols to assess the relative contribution of microbial vs. plant products to totalSOC. We found that grazing exclusion was associated with dramatically less overall belowground allocation, with lower root biomass, fine root exudates, and microbial biomass. Concurrently, grazed pasture contained greater totalSOC, and a larger fraction ofSOCthat originated from plant tissue deposition, suggesting that higher root litter deposition under grazing promotes greaterSOC. We conclude that grazing effects onSOCdepend on root system biomass, a pattern that may generalize to other C4‐dominated grasslands, especially in the subtropics. Improved understanding of ecological factors underlying root system biomass may be the key to forecastingSOCand optimizing grazing management to enhanceSOCaccumulation.

     
    more » « less
  2. Abstract From hillslope to small catchment scales (< 50 km 2 ), soil carbon management and mitigation policies rely on estimates and projections of soil organic carbon (SOC) stocks. Here we apply a process-based modeling approach that parameterizes the MIcrobial-MIneral Carbon Stabilization (MIMICS) model with SOC measurements and remotely sensed environmental data from the Reynolds Creek Experimental Watershed in SW Idaho, USA. Calibrating model parameters reduced error between simulated and observed SOC stocks by 25%, relative to the initial parameter estimates and better captured local gradients in climate and productivity. The calibrated parameter ensemble was used to produce spatially continuous, high-resolution (10 m 2 ) estimates of stocks and associated uncertainties of litter, microbial biomass, particulate, and protected SOC pools across the complex landscape. Subsequent projections of SOC response to idealized environmental disturbances illustrate the spatial complexity of potential SOC vulnerabilities across the watershed. Parametric uncertainty generated physicochemically protected soil C stocks that varied by a mean factor of 4.4 × across individual locations in the watershed and a − 14.9 to + 20.4% range in potential SOC stock response to idealized disturbances, illustrating the need for additional measurements of soil carbon fractions and their turnover time to improve confidence in the MIMICS simulations of SOC dynamics. 
    more » « less
  3. Abstract

    Predicting and mitigating changes in soil carbon (C) stocks under global change requires a coherent understanding of the factors regulating soil organic matter (SOM) formation and persistence, including knowledge of the direct sources of SOM (plants vs. microbes). In recent years, conceptual models of SOM formation have emphasized the primacy of microbial‐derived organic matter inputs, proposing that microbial physiological traits (e.g., growth efficiency) are dominant controls on SOM quantity. However, recent quantitative studies have challenged this view, suggesting that plants make larger direct contributions to SOM than is currently recognized by this paradigm. In this review, we attempt to reconcile these perspectives by highlighting that variation across estimates of plant‐ versus microbial‐derived SOM may arise in part from methodological limitations. We show that all major methods used to estimate plant versus microbial contributions to SOM have substantial shortcomings, highlighting the uncertainty in our current quantitative estimates. We demonstrate that there is significant overlap in the chemical signatures of compounds produced by microbes, plant roots, and through the extracellular decomposition of plant litter, which introduces uncertainty into the use of common biomarkers for parsing plant‐ and microbial‐derived SOM, especially in the mineral‐associated organic matter (MAOM) fraction. Although the studies that we review have contributed to a deeper understanding of microbial contributions to SOM, limitations with current methods constrain quantitative estimates. In light of recent advances, we suggest that now is a critical time to re‐evaluate long‐standing methods, clearly define their limitations, and develop a strategic plan for improving the quantification of plant‐ and microbial‐derived SOM. From our synthesis, we outline key questions and challenges for future research on the mechanisms of SOM formation and stabilization from plant and microbial pathways.

     
    more » « less
  4. Abstract

    Nitrogen (N) availability has been considered as a critical factor for the cycling and storage of soil organic carbon (SOC), but effects of N enrichment on the SOC pool appear highly variable. Given the complex nature of the SOC pool, recent frameworks suggest that separating this pool into different functional components, for example, particulate organic carbon (POC) and mineral‐associated organic carbon (MAOC), is of great importance for understanding and predicting SOC dynamics. Importantly, little is known about how these N‐induced changes in SOC components (e.g., changes in the ratios among these fractions) would affect the functionality of the SOC pool, given the differences in nutrient density, resistance to disturbance, and turnover time between POC and MAOC pool. Here, we conducted a global meta‐analysis of 803 paired observations from 98 published studies to assess the effect of N addition on these SOC components, and the ratios among these fractions. We found that N addition, on average, significantly increased POC and MAOC pools by 16.4% and 3.7%, respectively. In contrast, both the ratios of MAOC to SOC and MAOC to POC were remarkably decreased by N enrichment (4.1% and 10.1%, respectively). Increases in the POC pool were positively correlated with changes in aboveground plant biomass and with hydrolytic enzymes. However, the positive responses of MAOC to N enrichment were correlated with increases in microbial biomass. Our results suggest that although reactive N deposition could facilitate soil C sequestration to some extent, it might decrease the nutrient density, turnover time, and resistance to disturbance of the SOC pool. Our study provides mechanistic insights into the effects of N enrichment on the SOC pool and its functionality at global scale, which is pivotal for understanding soil C dynamics especially in future scenarios with more frequent and severe perturbations.

     
    more » « less
  5. Abstract

    To predict the behavior of the terrestrial carbon cycle, it is critical to understand the source, formation pathway, and chemical composition of soil organic matter (SOM). There is emerging consensus that slow‐cycling SOM generally consists of relatively low molecular weight organic carbon substrates that enter the mineral soil as dissolved organic matter and associate with mineral surfaces (referred to as “mineral‐associated OM,” or MAOM). However, much debate and contradictory evidence persist around: (a) whether the organic C substrates within the MAOM pool primarily originate from aboveground vs. belowground plant sources and (b) whether C substrates directly sorb to mineral surfaces or undergo microbial transformation prior to their incorporation into MAOM. Here, we attempt to reconcile disparate views on the formation of MAOM by proposing a spatially explicit set of processes that link plant C source with MAOM formation pathway. Specifically, because belowground vs. aboveground sources of plant C enter spatially distinct regions of the mineral soil, we propose that fine‐scale differences in microbial abundance should determine the probability of substrate–microbe vs. substrate–mineral interaction. Thus, formation of MAOM in areas of high microbial density (e.g., the rhizosphere and other microbial hotspots) should primarily occur through an in vivo microbial turnover pathway and favor C substrates that are first biosynthesized with high microbial carbon‐use efficiency prior to incorporation in the MAOM pool. In contrast, in areas of low microbial density (e.g., certain regions of the bulk soil), MAOM formation should primarily occur through the direct sorption of intact or partially oxidized plant compounds to uncolonized mineral surfaces, minimizing the importance of carbon‐use efficiency, and favoring C substrates with strong “sorptive affinity.” Through this framework, we thus describe how the primacy of biotic vs. abiotic controls on MAOM dynamics is not mutually exclusive, but rather spatially dictated. Such an understanding may be integral to more accurately modeling soil organic matter dynamics across different spatial scales.

     
    more » « less