Abstract
Vegetation restoration alters soil biotic and abiotic factors. Plants have evolved multiple strategies to adapt to nutrient limitation by reshaping and recruiting nutrient cycling-associated microbial communities in the rhizosphere. However, our understanding of the co-occurrence patterns of rhizosphere microbial communities and their role in soil multinutrient cycling during vegetation restoration remains limited. The present study explored the co-occurrence patterns of rhizosphere microbial communities along a chronosequence (15–45 years old) in Robinia pseudoacaciaplantations in China’s Loess Plateau region, the associations between core microbiota and multinutrient cycling under spatiotemporal changes. Our results indicate that soil multifunctionality influences microbial co-occurrence patterns in the R. pseudoacacia rhizosphere, resulting in a more stable bacterial network than fungal network, forest age was a major driver of modularized distribution of nodes in bacterial and fungal networks, and forest age-sensitive microbes were taxonomically diverse at the phylum level. Meanwhile, we found that core microbiota play essential role in rhizosphere soil multinutrient cycling under R. pseudoacacia afforestation.
Keywords : Rhizosphere soil;Robinia pseudoacacia;Microbial community; Co-occurrence network.
Introduction
Soil microorganisms shape aboveground biodiversity and the functioning of terrestrial ecosystems significantly. They also play a key role in determining the ecological and evolutionary responses of terrestrial ecosystems to current and future environmental change (6). The rhizosphere, a narrow zone where plant and soil interact, is intriguingly complex and dynamic, and recruits numerous microorganisms (43). The assembly processes of rhizosphere microbial communities are governed by both abiotic and biotic factors. Root exudates (2, 21, 39), soil properties (1, 23, 45), plant type and development stage (30), and fine roots (34) are major factors driving the assembly and differentiation of rhizosphere microbial communities (7). Plant–soil microbe feedback refers to the linkages between plants and soil microbial communities. Plant root exudates contain secondary metabolites with plant-defense functions that alter root-associated microbial community structure and facilitate plant growth (22). Plants modify their exudation patterns to adapt to microbial nutrient demands, which in turn facilitates the meeting of plant nutrient demands during different growth stages (55). Therefore, survival of any plant species in a particular rhizosphere environment depends primarily on the capacity of the plant to perceive changes in the local environment that require adaptive responses (50).
Characterization of soil microbial community structure is often used to determine the responses of soil to disturbance and assess ecosystem stability (3). The functions of ecosystems are diverse rather than specific. Since Hector and Bagchi (19) proposed the quantification of ecosystem multifunctionality in 2007, numerous researchers have focused on the issue. Evidence from research suggests a close relationship between soil microbial diversity and ecosystem multifunctionality in different environments (11, 49). Delgado-Baquerizo et al. (11) collected soil samples from 179 locations in 78 global drylands across Scotland and observed that soil microbial diversity increased with an increase in ecosystem multifunctionality. Furthermore, Jiao et al. (26) reported that soil bacterial α-diversity and β-diversity were correlated with ecosystem multifunctionality in maize and rice soils, respectively, on a continental scale. Because the rhizosphere is a hotspot of microbial activity, stable structure and functioning of rhizosphere microbial communities (plant–root–soil and associated microbes–hyphae) are conducive to the activation, absorption, and utilization of soil nutrients. They are also essential for achieving multi-interface interactions and synergies, while facilitating the addressing of the problems associated with food security and environmental protection (47)(Shen et al, 2021).
Black locust (Robinia pseudoacacia ) is one of the major afforestation species in China’s Loess Plateau region, and it is of great significance for ecological restoration and water and soil conservation. Some studies have reported that soil properties and microbial community structure vary along the chronosequence in R. pseudoacacia plantations. Particularly,R . pseudoacacia afforestation altered soil bacterial richness and community composition in a forest stand aged 25 years (37). Moreover, restoration time and vegetation type (abandoned land vs.R. pseudoacacia plantation) markedly influenced soil physical properties, nutrient contents, and microbial biomass (54). Furthermore, rhizosphere microbial community structure are influenced by soil properties and fine root parameters in R. pseudoacaciaplantations. Soil available phosphorus (AP) contents have been reported to be lower at forest ages of 25 and 35 years than at forest ages of 5 and 15 years, with soil AP and total phosphorus (TP) contents of fine roots being the key factors regulating rhizosphere microbial community structure in the root–soil system following Robiniaafforestation (35).
Currently, there is a need to observe the trends in rhizosphere microbial community structure along a chronosequence during vegetation restoration. Because rhizosphere microbiota could respond rapidly to changes in environmental conditions induced by ecological restoration, their turnover dynamics could serve as sensitive indicators that could facilitate the monitoring of the restoration process (3). Despite numerous studies having been carried out on soil microbial diversity inR. pseudoacacia plantations (Castellano et al., 2021; Hamonts et al., 2018; Lemanceu et al., 2017), little is known about the assembly process of rhizosphere microbial communities and their co-occurrence network patterns along a chronosequence. In addition, although the changes in soil factors along a chronosequence are well documented (Hamonts et al., 2018; Castellano et al., 2021), the relationship between ecosystem functionality and rhizosphere microbial community structure (especially core microbiota) inR. pseudoacacia plantations is poorly understood. Such a poor understanding of rhizosphere community dynamics along a chronosequence in R. pseudoacacia plantations calls for the exploration of the role of core microbiota in the interaction interfaces in the rhizosphere through the identification core microbial taxa and predicting their contribution to soil nutrient cycling activities.
Core microbiota refer to the major microbial components present in the general community that are enriched, selected, and inherited through evolutionary processes (32). Core microbiota sustain plant health and increase productivity (15). In addition, core rhizosphere microbiota (rhizobiome) have greater effects on soil nutrient cycling and plant growth than other rhizobiomes in the rhizosphere (8). It has been reported that soil bacterial community composition shifted fromAcidobacteria- dominated to Proteobacteria- dominated and then Acidobacteria- dominated communities with an increase inR. pseudoacacia forest age, whereas fungal communities were dominated by Ascomycta and Zygomycota irrespective of forest age (36, 37). However, the previous studies did not elucidate the potential relationships between the dominant microbes and soil multifunctionality, in addition to their role in the microbial network. Therefore, it is required to identify core microbiota and predict their contribution to rhizosphere soil nutrient cycling, which is essential for the implementation of rational rhizosphere management strategies and maximizing microbiota ecological function.
Here, we present a rhizosphere soil survey conducted in R. pseudoacacia plantations across different forest ages at the Huaiping Forest Farm in Yongshou, Shaanxi Province, China. We analyzed bacterial and fungal diversity using high-throughput sequencing technologies and quantified rhizosphere soil multifunctionality based on measurements of edaphic variables associated with nutrient cycling. The aims of the present study were to (i) explore rhizosphere microbial diversity and the driving factors along a chronosequence in the course of R. pseudoacaciavegetation restoration; (ii) explore the influence of forest age on the co-occurrence patterns of rhizosphere microbes and the network features of forest age-sensitive microbes; and (iii) identify core microbiota and their potential contribution to rhizosphere soil multinutrient cycling in R. pseudoacacia plantations.
Materials and methods