A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment

Abstract

Highly diverse microbial assemblages colonize plant roots. It is still poorly understood whether different members of this root microbiome act synergistically by supplying different services (for example, different limiting nutrients) to plants and plant communities. In order to test this, we manipulated the presence of two widespread plant root symbionts, arbuscular mycorrhizal fungi and nitrogen-fixing rhizobia bacteria in model grassland communities established in axenic microcosms. Here, we demonstrate that both symbionts complement each other resulting in increased plant diversity, enhanced seedling recruitment and improved nutrient acquisition compared with a single symbiont situation. Legume seedlings obtained up to 15-fold higher productivity if they formed an association with both symbionts, opposed to productivity they reached with only one symbiont. Our results reveal the importance of functional diversity of symbionts and demonstrate that different members of the root microbiome can complement each other in acquiring different limiting nutrients and in driving important ecosystem functions.

Figure 1

Productivity and diversity of microcosms. The productivity of the microcosms (a) is reported with the dry weight shoot biomass (sum of the three harvests) for the three plant functional groups (legumes, herbs and grasses) and the biomass of the roots at the third harvest. Plant diversity (b) is based on the shoot biomass data of the three harvests. Grassland microcosms contained no plant symbionts (C), only rhizobia (R), only AM fungi (M) or both symbionts (MR). Bars represent means (n=9; ±s.e.m.) and letters (in a are colored by functional group) indicate statistical significance; treatments not sharing a letter differ at P<0.05 (Tukey's HSD). The total productivity of the microcosms (shoot and roots combined) was not significantly different among the treatments. Statistic details are given in Supplementary Table S1.

Figure 2

Plant community composition. The heatmap reports the dry weight shoot biomass of individual plant species (in rows) in all microcosms (in columns). The data comprise the summed productivity of the three harvests and are presented with a log scale. Dendrograms report similarities in productivity of the different plant species (left of the heatmap) and in the differentially treated microcosms (above the heatmap) based on complete linkage clustering using Pearson distances. Microcosms containing no plant symbionts (C), only rhizobia (R), only AM fungi (M), or both symbionts (MR) as well as the plant functional groups are marked as indicated.

Figure 3

Plant nutrient acquisition. P content (a) and mineral and symbiotically fixed N content (b) in plants of the grassland microcosms containing no plant symbionts (C), only rhizobia (R), only AM fungi (M), both symbionts (MR). Total plant nutrient content (shoot and roots combined) refers to the overall plant nutrient uptake in the microcosms (sum of the three harvests). Bars represent means (n=9;±s.e.m.) and letters indicate statistical significance; treatments not sharing a letter differ at P<0.05 (Tukey's HSD). Statistic details and the nutrient acquisition data per functional groups are reported in Supplementary Table S1 and Supplementary Figure S6, respectively.

Figure 4

Seedling establishment. After 11 months, seedlings were added between the plants, i.e., into the established grasslands microcosms containing no plant symbiont (C), only rhizobia (R), only AM fungi (M), or both symbionts (MR). Seedling establishment was approximated for each developing plant individual with the shoot dry weight of the biomass harvested 5.5 months later at the third harvest. Plant species and their functional groups are indicated. Bars represent means (n=9; ±s.e.m.), letters below the bars indicate statistical significance; treatments not sharing a letter differ at P<0.05 (Tukey's HSD) and statistical details are given in Supplementary Table S1.