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