Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls

Abstract

Soil organic matter (SOM) and the carbon and nutrients therein drive fundamental submicron- to global-scale biogeochemical processes and influence carbon-climate feedbacks. Consensus is emerging that microbial materials are an important constituent of stable SOM, and new conceptual and quantitative SOM models are rapidly incorporating this view. However, direct evidence demonstrating that microbial residues account for the chemistry, stability and abundance of SOM is still lacking. Further, emerging models emphasize the stabilization of microbial-derived SOM by abiotic mechanisms, while the effects of microbial physiology on microbial residue production remain unclear. Here we provide the first direct evidence that soil microbes produce chemically diverse, stable SOM. We show that SOM accumulation is driven by distinct microbial communities more so than clay mineralogy, where microbial-derived SOM accumulation is greatest in soils with higher fungal abundances and more efficient microbial biomass production.

Figure 1. Soil development and organic matter chemistry.

Images of sugar-treated model soils over time (a); the far left panel is an uninoculated sterile kaolinite and sand mixture, and the far right panel is the same mixture, inoculated and treated with weekly glucose additions for 15 months. Relative abundance of chemical compound groups in substrate (Time 0) and model soils amended with (b) sugar, (c) syringol and (d) plant dissolved organic carbon (DOC). These are compared to soil collected from an agricultural field (e). Glucose and cellobiose treatments were averaged since there were no significant differences in their chemistry (ANOVA: P>0.05). Numbers above bars are the total number of identified compounds.

Figure 2. Differences in soil organic matter chemistry between substrate and clay types.

Non-metric multidimensional scaling (NMDS) ordination of the relative abundance of chemistry compounds at 18 months for substrate and clay treatments. Open symbols are kaolinite and closed symbols are montmorillonite. For comparison, unprocessed substrates (Time 0) and an agricultural field soil are indicated by a star symbol (Stress=8.1, Monte Carlo: P<0.05).

Figure 3. Influence of substrate and clay type on soil microbial communities and microbial growth efficiency.

Substrate treatment differences in the relative abundance (RA) of fungi (a), Gram-negative bacteria (b), Gram-positive bacteria (c) at 15 months, and microbial carbon use efficiency (CUE) for kaolinite (d) and montmorillonite (e) model soils. The CUE values (d,e) are for 9 and 15 months of incubation. Significant substrate treatment effects are within clay type or within time and are indicated by different letters (ANOVA: P<0.05). Error bars represent one s.e. (experimental replication n=5).

Figure 4. Relationships between soil organic matter and microbial variables.

Non-metric multidimensional scaling (NMDS) ordination of accumulated SOC at 12, 15 and 18 months for sugar- and syringol-treated soils (a) and Pearson correlations for fungal relative abundances and microbial carbon use efficiency (CUE) (b), SOC and CUE (c), and fungal relative abundances and SOC (d) at 15 months. NMDS points are categorized post hoc based on soil C concentrations at 18 months: high SOC (closed circles), medium SOC (closed squares) and low SOC (closed triangles) (Stress=4.2, Monte Carlo: P=0.019, multi-response permutation procedure for SOC groups: T=−10.037, A=0,469, P<0.0001). NMDS table inset is Pearson correlation r values with ordination Axis 1.