Functional diversity of microbial decomposers facilitates plant coexistence in a plant-microbe-soil feedback model

Abstract

Theory and empirical evidence suggest that plant-soil feedback (PSF) determines the structure of a plant community and nutrient cycling in terrestrial ecosystems. The plant community alters the nutrient pool size in soil by affecting litter decomposition processes, which in turn shapes the plant community, forming a PSF system. However, the role of microbial decomposers in PSF function is often overlooked, and it remains unclear whether decomposers reinforce or weaken litter-mediated plant control over nutrient cycling. Here, we present a theoretical model incorporating the functional diversity of both plants and microbial decomposers. Two fundamental microbial processes are included that control nutrient mineralization from plant litter: (i) assimilation of mineralized nutrient into the microbial biomass (microbial immobilization), and (ii) release of the microbial nutrients into the inorganic nutrient pool (net mineralization). With this model, we show that microbial diversity may act as a buffer that weakens plant control over the soil nutrient pool, reversing the sign of PSF from positive to negative and facilitating plant coexistence. This is explained by the decoupling of litter decomposability and nutrient pool size arising from a flexible change in the microbial community composition and decomposition processes in response to variations in plant litter decomposability. Our results suggest that the microbial community plays a central role in PSF function and the plant community structure. Furthermore, the results strongly imply that the plant-centered view of nutrient cycling should be changed to a plant-microbe-soil feedback system, by incorporating the community ecology of microbial decomposers and their functional diversity.

Fig. 1.

Flow diagram of the plant–microbe–soil feedback model. Flows from the inorganic nutrient pool (N) to the plant compartments (P_L and P_N) represent primary production processes. Flows from the plant compartments to the two litter compartments (D_R and D_S) represent litter production. Flows from the litter compartments to the microbial biomasses (M_R and M_S) represent decomposition (gross mineralization) and subsequent microbial immobilization (microbial growth) processes. Flows from the litter compartments to the inorganic nutrient pool represent direct mineralization. Flows from the microbial biomass to the inorganic nutrient pool represent net mineralization through nutrient release from microbial biomass due to predation.

Fig. 2.

Consequences of PMSF on nutrient cycling, as a function of plant litter decomposability. (A) Relationship between litter decomposability (f_L) and equilibrium nutrient pool size in systems with a better competitor for light (P_L) only. Red, green, and blue lines correspond to systems with only M_R, only M_S, and both M_R and M_S, respectively. In the region with coexisting M_R and M_S, the slope of the line is zero. (B) Relationship between litter decomposability (f_L), relative abundance of D_R-preferring microbes (RA of M_R, dimensionless), and readily decomposable D_R and slowly decomposable D_S accumulations in a system with P_L only. (C) Relationship between the average litter decomposability (long-term average of , from t = 45,000 to t = 50,000) and the average nutrient pool size (long-term average of N) in a system with two plant species. Consequences of PMSF on nutrient pool size for every combination of (f_L and f_N) from (0.0, 0.0) to (1.0, 1.0) with interval (Δf_L, Δf_N) = (0.01, 0.01) are plotted against the average litter decomposability in a system with microbial functional group M_R only (red dots), M_S only (green dots), and with two competing microbial groups (blue dots). All parameters are set as default values (Table S1).

Fig. 3.

Roles of microbial diversity in determining the sign of PSF. Dependence of the sign of PSF on litter decomposabilities f_L and f_N is shown in a system with P_L only (“P_L-dominant community”) (A) and P_N only (“P_N-dominant community”) (B), respectively. There are three distinct configurations for the microbial community: a system with M_R only (“w/ M_R only”), M_S only (“w/ M_S only”), and with microbial diversity (“w/ diversity”). The sign of PSF is positive (“Positive PSF”, ”Positive”, “+tive”, or “+”) or negative (“Negative PSF” or “Negative”). In a system with microbial diversity, the realized microbial composition depending on litter decomposability is shown as “Shifts in microbial composition” (M_S, M_R and M_S, or M_R). If the litter decomposability is too low, the system cannot persist (“no persistence”). Parameters are set to default values (Table S1).

Fig. 4.

Consequences of PMSF on plant communities, as a function of the plant litter decomposability (f_L and f_N). (A and B) Microbial community consisting of M_R (A) or M_S (B) only. (C) Microbial community consisting of M_R and M_S, and their realized community compositions as determined by PMSF. A better competitor for light (P_L) is dominant in the plant community in region L, a better competitor for nutrient (P_N) is dominant in region N, and the two plant species coexist in the region C. In region X, the ecosystem cannot persist because the plant litter decomposability of the dominant species or that of the invasible species is too low (see SI Text, Section 5). Coexistence or dominance of P_N is realized in region C or N, and dominance of P_L or P_N is realized in region L or N, depending on the initial conditions. In a system with functional microbial diversity, dependence of the realized microbial composition (dominance of D_R- or D_S-preferring microbes or coexistence) on litter decomposability is not shown (Fig. S6). Although plant coexistence is realized by periodic succession with some combinations of litter decomposability, we did not distinguish this from coexistence at steady state. The presence of periodic succession may result in complex boundaries between region C or N, region N, and region L or N (see SI Text, Section 5). Parameters are set to default values (Table S1).