Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity

Abstract

Species-rich plant communities have been shown to be more productive and to exhibit increased long-term soil organic carbon (SOC) storage. Soil microorganisms are central to the conversion of plant organic matter into SOC, yet the relationship between plant diversity, soil microbial growth, turnover as well as carbon use efficiency (CUE) and SOC accumulation is unknown. As heterotrophic soil microbes are primarily carbon limited, it is important to understand how they respond to increased plant-derived carbon inputs at higher plant species richness (PSR). We used the long-term grassland biodiversity experiment in Jena, Germany, to examine how microbial physiology responds to changes in plant diversity and how this affects SOC content. The Jena Experiment considers different numbers of species (1-60), functional groups (1-4) as well as functional identity (small herbs, tall herbs, grasses, and legumes). We found that PSR accelerated microbial growth and turnover and increased microbial biomass and necromass. PSR also accelerated microbial respiration, but this effect was less strong than for microbial growth. In contrast, PSR did not affect microbial CUE or biomass-specific respiration. Structural equation models revealed that PSR had direct positive effects on root biomass, and thereby on microbial growth and microbial biomass carbon. Finally, PSR increased SOC content via its positive influence on microbial biomass carbon. We suggest that PSR favors faster rates of microbial growth and turnover, likely due to greater plant productivity, resulting in higher amounts of microbial biomass and necromass that translate into the observed increase in SOC. We thus identify the microbial mechanism linking species-rich plant communities to a carbon cycle process of importance to Earth's climate system.

Keywords: microbial activity; microbial carbon use efficiency; microbial necromass; microbial turnover; plant diversity; soil organic carbon.

Figure 1

Conceptual model depicting the hypothetical relationships between plant species richness and microbial physiology that are expected to promote soil organic carbon (SOC) build‐up in species‐rich plant communities (pool sizes within, microbial processes without text frames; mic, microbial; CUE, carbon use efficiency)

Figure 2

Linear regressions of plant species richness (log) and soil, plant, and microbial parameters. (a) Soil organic carbon is in mg/g soil dry weight (DW), (b) root carbon (log) in g/m² soil, (c) microbial growth (sqrt) in µg microbial biomass carbon g⁻¹ soil DW day⁻¹, (d) microbial respiration in µg CO₂‐carbon g⁻¹ soil DW day⁻¹, (e) microbial CUE is in absolute fractions, (f) biomass‐specific growth (log) in ng carbon growth µg⁻¹ microbial biomass carbon day⁻¹, (g) microbial biomass carbon in µg/g soil DW, (h) total microbial necromass in mg necromass carbon/g soil DW, and (i) fungal:bacterial necromass ratio (log) represents fungal necromass carbon divided by bacterial necromass carbon. Significance levels are indicated by asterisks (*p ≤ .05, **p ≤ .01, ***p ≤ .001) and significant relationships are presented by solid lines; p values are given in brackets next to the adjusted R ² value if p ≤ .1, with dashed lines

Figure 3

Structural equation model (piecewise SEM) of plant species richness (PSR log), microbial activity (Growth_mic, microbial growth; Respiration_mic, microbial respiration), and biomass (root C, root carbon; C_mic, microbial biomass carbon) as predictors for soil organic carbon (SOC) (C₁₄ = 11.36, p = .657). Arrows show significant paths (p ≤ .05), numbers next to them are standardized path coefficients with asterisks indicating their significance (*p ≤ .05, **p ≤ .01, ***p ≤ .001). Numbers in the boxes of endogenous variables are the explained variances of fixed (R ² _m) and fixed plus random factors (R ² _c)