Biodiversity of network modules drives ecosystem functioning in biochar-amended paddy soil

Abstract

Introduction: Soil microbes are central in governing soil multifunctionality and driving ecological processes. Despite biochar application has been reported to enhance soil biodiversity, its impacts on soil multifunctionality and the relationships between soil taxonomic biodiversity and ecosystem functioning remain controversial in paddy soil.

Methods: Herein, we characterized the biodiversity information on soil communities, including bacteria, fungi, protists, and nematodes, and tested their effects on twelve ecosystem metrics (including functions related to enzyme activities, nutrient provisioning, and element cycling) in biochar-amended paddy soil.

Results: The biochar amendment augmented soil multifunctionality by 20.1 and 35.7% in the early stage, while the effects were diminished in the late stage. Moreover, the soil microbial diversity and core modules were significantly correlated with soil multifunctionality.

Discussion: Our analysis revealed that not just soil microbial diversity, but specifically the biodiversity within the identified microbial modules, had a more pronounced impact on ecosystem functions. These modules, comprising diverse microbial taxa, especially protists, played key roles in driving ecosystem functioning in biochar-amended paddy soils. This highlights the importance of understanding the structure and interactions within microbial communities to fully comprehend the impact of biochar on soil ecosystem functioning in the agricultural ecosystem.

Keywords: biochar amendment; core modules; ecosystem functioning; protists; soil microbial biodiversity.

FIGURE 1

The multifunctionality in different treatments. (A) Early stage of rice growing, (B) late stage of rice growing. CK, control, and without additive; B1, with the addition of 2.5 g kg^–1 biochar; B2, with the addition of 5 g kg^–1 biochar; B3, with the addition of 10 g kg^–1 biochar; L: large macroaggregates, S, small macroaggregates, M, microaggregates. P-values were indicated by asterisks: *P < 0.05, **P < 0.01, ***P < 0.001, and ****P < 0.0001.

FIGURE 2

The relationship between multifunctionality and biodiversity of organisms with biochar addition. (A–D) The linear relationships between multifunctionality and the biodiversity of selected groups of soil organisms (averaged standardized between 0 and 1). Statistical analysis was performed using ordinary least squares linear regressions; P-values were indicated by asterisks: *P < 0.05, **P < 0.01, and ***P < 0.001. (E) Significant correlations (Spearman; ρ < 0.05) between the diversity of single groups of organisms and 12 single ecosystem metrics (including functions related to enzyme activities, nutrient provisioning, and element cycling). SOC, soil organic carbon; TN, total nitrogen; TP, total phosphorus; DOC, dissolved organic carbon; AS, available sulfur.

FIGURE 3

The main modules in the network and the OTU number proportion in the modules. (A) Co-occurrence network of soil microbial OTUs. Co-occurrence networks visualizing significant correlations (Spearman’s correlation coefficient >0.65) between OTUs in the communities of four kinds of soil microbial taxa (bacteria, fungi, protists, and nematodes). Four modules in microbial networks are shown in different colors. The size of each node accounts for the degree of OTUs, representing the connectedness among OTUs. The connecting lines (edges) among those nodes represent the interactions between soil organisms. The red and blue edges show positive and negative interactions, respectively. (B) OTUs number proportion (%) of the soil organismal phylotypes in Modules 1–4 in the network.

FIGURE 4

The main modules and the correlation between modules and physicochemical properties. (A–D) Taxonomic composition of modules. The different soil organisms are shown in different colors. The size of each node accounts for the degree of OTUs, representing the connectedness among OTUs. The connecting lines among those nodes represent the interactions between soil organisms. (E) Significant correlations (ρ < 0.05) between the modules and single ecosystem functions. P-values were indicated by asterisks: *P < 0.05, **P < 0.01, ***P < 0.001, and ****P < 0.0001.

FIGURE 5

The correlation between the four main modules and multifunctionality. Statistical analysis was performed using ordinary least squares linear regressions.

FIGURE 6

The correlation between the main protists in four modules, protistan functional groups, and multifunctionality. Significant correlations (Spearman, ρ < 0.05) between protists within each module, as well as between different protistan functional groups and ecosystem functions. P-values were indicated by asterisks: *P < 0.05, **P < 0.01, ***P < 0.001, and ****P < 0.0001.

FIGURE 7

Structural equation models (SEMs) accounting for the direct and indirect relationships between biochar, modules, soil biodiversity, and multifunctionality. (A) Structural equation model describing the relationship between soil biodiversity (bacteria, fungi, protists, and nematode) and multifunctionality. (B) Structural equation model describing the correlation between modules and multifunctionality. The blue and red lines indicate positive and opposite effects, respectively. The black lines show no significant impact. The thickness of the line infers the strength of the relationship. Asterisks indicate the significance level of each coefficient: P-values: *p < 0.05, **p < 0.01, and ***p < 0.001.