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. 2022 Mar 9;13(1):1229.
doi: 10.1038/s41467-022-28715-9.

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

Matthew E Craig  1   2 , Kevin M Geyer  3   4 , Katilyn V Beidler  5 , Edward R Brzostek  6 , Serita D Frey  3 , A Stuart Grandy  3 , Chao Liang  7 , Richard P Phillips  5
Affiliations

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

Matthew E Craig et al. Nat Commun. .

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.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Conceptual model and map of study sites.
a Conceptual model showing microbe-mediated mechanisms of mineral-associated soil organic carbon (SOC) formation and decay. Pathway 1 represents the necromass stabilization hypothesis and we note that different types of necromass may be differentially susceptible to mineral stabilization. Other numbers represent (2) mineral stabilization of plant inputs without assimilation by microbes, (3) mineral stabilization of microbial extracellular compounds, (4) stimulation of microbe-mediated mineral-associated SOC decay, (5) and the role of soil properties in governing mineral-associated SOC accumulation. b Map of study sites including Wabikon Lake Forest (WLF), Harvard Forest (HF), Lilly-Dickey Woods (LDW), Smithsonian Conservation Biology Institute (SCBI), Smithsonian Environmental Research Center (SERC), and Tyson Research Center (TRC).
Fig. 2
Fig. 2. Microbial physiological traits and mineral-associated SOC (MA-SOC) formation in the microcosm experiment.
a Linear relationship (±SE; n = 16) between the litter quality index (PC1 in Fig. S1A) and the microbial physiological trait index (PC1 in Fig. S1B) after 15 days (Early stage: R2 = 0.14; P = 0.16) and 100 days (Intermediate stage: R2 = 0.38; P = 0.01) of decomposition, (b) lack of a relationship (P > 0.96) between the microbial physiological trait index and litter-derived MA-SOC after 30 (Early) and 185 days (Intermediate), and (c) path analysis showing the direct and indirect effects of the litter quality index (Litter quality) on the percentage of added litter C recovered in mineral-associated SOC (Litter-derived MA-SOC). Indirect effects of litter quality are mediated through the microbial physiological trait index. Numbers above and below paths represent standardized coefficients during early- and intermediate-stage decomposition, respectively, with significance levels indicated (*p < 0.1, **p < 0.05, and ***p < 0.01). Thickness and color of lines correspond to coefficient magnitude and direction, respectively. Total and indirect effects of litter quality on soil C formation are also summarized with standardized coefficients.
Fig. 3
Fig. 3. Soil-derived (i.e., pre-existing) carbon losses in the microcosm experiment.
a Path analysis showing the direct and indirect effects of the litter quality index (Litter quality) on soil-derived mineral-associated SOC (MA-SOC). Indirect effects of litter quality are mediated through the microbial physiological trait index. Numbers above and below paths represent standardized coefficients during early- and intermediate-stage decomposition, respectively, with significance levels indicated (*p < 0.1, **p < 0.05, and ***p < 0.01). Thickness and color of lines correspond to coefficient magnitude and direction, respectively. Total and indirect effects of litter quality on soil C formation are also summarized with standardized coefficients. b Linear relationship (±SE; n = 16) between the litter nitrogen index—i.e., the second axis of the litter quality PCA which correlated negatively with litter C:N and AUR:N (Fig. S1A)—and cumulative soil-derived respiration (CO2-C) after 30 days (Early: R2 = 0.59; P < 0.01) and 185 days of decomposition (Intermediate: R2 = 0.32; P = 0.02).
Fig. 4
Fig. 4. Results from the field study.
Linear mixed model coefficients relating the percentage of soil C stored in mineral-associated SOC (a) and total microbial necromass (b) to the litter quality index (Litter quality; PC1 in Fig. S1C) the microbial physiological trait index (Mic. phys. traits; PC1 in Fig S1D), fine root biomass, soil pH, oxalate-extractable iron (Fe-ox), and soil clay content. Plot shows standard error (n = 54; inner bold lines) and 95% confidence intervals (outer lines). Coefficients were centered and standardized to show the relative importance of each predictor despite the different scales on which the variables were measured. Black points indicate p < 0.1.
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