Tree and shrub richness modifies subtropical tree productivity by regulating the diversity and community composition of soil bacteria and archaea

Abstract

Background: Declines in plant biodiversity often have negative consequences for plant community productivity, and it becomes increasingly acknowledged that this may be driven by shifts in soil microbial communities. So far, the role of fungal communities in driving tree diversity-productivity relationships has been well assessed in forests. However, the role of bacteria and archaea, which are also highly abundant in forest soils and perform pivotal ecosystem functions, has been less investigated in this context. Here, we investigated how tree and shrub richness affects stand-level tree productivity by regulating bacterial and archaeal community diversity and composition. We used a landscape-scale, subtropical tree biodiversity experiment (BEF-China) where tree (1, 2, or 4 species) and shrub richness (0, 2, 4, 8 species) were modified.

Results: Our findings indicated a noteworthy decline in soil bacterial α-diversity as tree species richness increased from monoculture to 2- and 4- tree species mixtures, but a significant increase in archaeal α-diversity. Additionally, we observed that the impact of shrub species richness on microbial α-diversity was largely dependent on the level of tree species richness. The increase in tree species richness greatly reduced the variability in bacterial community composition and the complexity of co-occurrence network, but this effect was marginal for archaea. Both tree and shrub species richness increased the stand-level tree productivity by regulating the diversity and composition of bacterial community and archaeal diversity, with the effects being mediated via increases in soil C:N ratios.

Conclusions: Our findings provide insight into the importance of bacterial and archaeal communities in driving the relationship between plant diversity and productivity in subtropical forests and highlight the necessity for a better understanding of prokaryotic communities in forest soils. Video Abstract.

Keywords: Archaea; BEF-China; Bacteria; Shrub competition; Tree growth; Tree species richness.

Fig. 1

Sampling and experimental design. a Plots with tree species richness gradients (1, 2, 4) and shrub species richness gradients (0, 2, 4, 8) selected from BEF-China platform (site A, site B). b The tree species and their combinations used in this study

Fig. 2

Soil bacterial and archaeal α-diversity and community structure. a tree richness and shrub richness effects on soil microbial α-diversity; b tree richness and shrub richness effects on soil microbial β-dissimilarity. The asterisks showed the p-value significance level, *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001 and ns showed no significance

Fig. 3

Pairwise correlation matrix of environmental factors with Mantel tests of bacterial and archaeal communities. Red and blue lines indicate positive and negative correlations, respectively, while solid and dashed lines indicate the significant correlations (p < 0.05) and insignificant correlations (p > 0.05)

Fig. 4

A general overview of changes in taxonomic composition and species abundance for bacterial and archaeal communities affected by increased plant species richness. a the relative of phylum-level taxa dominated across tree species richness and shrub species richness levels; b bipartite networks illustrating the specific and conserved amplicon sequence variants (ASVs) assigned to monoculture, two-species mixtures, and four-species mixtures and their combinations, respectively for soil bacterial and archaeal community; c volcano plots showing up- and down-regulated ASVs in three comparisons: tree richness of 1 and 2, tree richness 1and 4, tree richness of 2 and 4. An adjusted p value < 0.01 is indicated in red, while an adjusted p value < 0.01 is indicated in black. The top ten ASVs with the most significant differences in abundance were indicated by their ID numbers and the numbers of ASVs with significantly differences in abundance for the three comparisons are indicated in bracket

Fig. 5

The co-occurrence networks of bacterial communities (a) and archaeal communities (b) in three tree species richness levels, monocultures, two-species mixtures and four species-mixtures, respectively. The nodes in the networks are colored according to the taxonomic assignments at phylum level and the size of each node is proportional to the relative abundance

Fig. 6

Plant richness affects tree productivity by regulating soil properties and microbial communities. a Stand-level tree volume increment as a function of aboveground plant richness from 2017–2018. b Structural equation models demonstrating the direct and indirect effects of aboveground plant richness on soil nutrient contents, microbial communities and community-level tree productivity, red arrows indicate significant and positive relationships (p < 0.05), and dashed arrows indicate connections with insignificant relationship (p > 0.05). TC: total carbon, TN: total nitrogen, TP: total phosphorus, SM: soil moisture, C/N: the ratio of soil organic C and N, MBC/C_org: the ratio of microbial biomass C and soil organic C