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Article

Successions of Bacterial and Fungal Communities in Biological Soil Crust under Sand-Fixation Plantation in Horqin Sandy Land, Northeast China

by
Chengyou Cao
1,2,*,
Ying Zhang
1,2 and
Zhenbo Cui
1,2
1
College of Life and Health Sciences, Northeastern University, Shenyang 110169, China
2
Liaoning Province Key Laboratory of Bioresource Research and Development, Northeastern University, Shenyang 110169, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(9), 1631; https://doi.org/10.3390/f15091631
Submission received: 12 August 2024 / Revised: 7 September 2024 / Accepted: 13 September 2024 / Published: 15 September 2024
(This article belongs to the Section Forest Soil)
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Abstract

:
Biological soil crusts (BSCs) serve important functions in conserving biodiversity and ecological service in arid and semi-arid regions. Afforestation on shifting sand dunes can induce the formation of BSC on topsoil, which can accelerate the restoration of a degraded ecosystem. However, the studies on microbial community succession along BSC development under sand-fixation plantations in desertification areas are limited. This paper investigated the soil properties, enzymatic activities, and bacterial and fungal community structures across an age sequence (0-, 10-, 22-, and 37-year-old) of BSCs under Caragana microphylla sand-fixation plantations in Horqin Sandy Land, Northeast China. The dynamics in the diversities and structures of soil bacterial and fungal communities were detected via the high-throughput sequencing of the 16S and ITS rRNA genes, respectively. The soil nutrients and enzymatic activities all linearly increased with the development of BSC; furthermore, soil enzymatic activity was more sensitive to BSC development than soil nutrients. The diversities of the bacterial and fungal communities gradually increased along BSC development. There was a significant difference in the structure of the bacterial/fungal communities of the moving sand dune and BSC sites, and similar microbial compositions among different BSC sites were found. The successions of microbial communities in the BSC were characterized as a sequential process consisting of an initial phase of the faster recoveries of dominant taxa, a subsequent slower development phase, and a final stable phase. The quantitative response to BSC development varied with the dominant taxa. The secondary successions of the microbial communities of the BSC were affected by soil factors, and soil moisture, available nutrients, nitrate reductase, and polyphenol oxidase were the main influencing factors.

1. Introduction

Biological soil crusts (BSCs) are assemblages of microorganisms (including cyanobacteria, bacteria, and fungi), lichens and mosses, and surface soil particles; they are widely distributed in arid and semi-arid lands [1,2]. Based on differences in their dominant components (bacteria, fungi, cyanobacteria/algal, lichen, or moss), BSCs can be classified into different succession stages [3,4]. BSCs are important for the function of arid and semi-arid ecosystems, and their effects on stabilizing soil surface, resisting wind erosion, increasing fertility, altering hydrological cycle, and affecting runoff infiltration are well documented [5,6,7,8,9], which confirms that the formation and development of BSCs can accelerate the restoration of desertified ecosystems. In desert areas, BSCs may play more important roles in conserving biodiversity and ecological services. The formation mechanism and estimated recovery rate of BSC in desertification areas have been studied [1,10,11,12]. The results indicate that the formation and development of BSC are affected by vegetation, soil property, and plant–soil-microbe interactions; several decades are needed for the complete recovery of all the components of degraded BSC communities in desertified lands [10,13]. Some studies also suggest that revegetation on moving sand land or the inoculation of soils carrying the main components of BSC may induce and facilitate the development of BSC on the surface of sandy soil [10,14]. Most previous relative studies have paid more attention to the composition and function of BSCs in different natural habitats. By contrast, studies on BSC development in artificially planted sand-fixation plantations in desertification areas are limited. Information on the composition dynamic of BSC communities in revegetation areas is required in order to better understand the restoration mechanisms of degraded sand land ecosystems and plant–soil-microbe interactions.
Horqin Sandy Land lies in the semi-arid agropastoral steppe of northern China, and has been historically characterized as an extended steppe–woodland landscape. However, it has suffered serious desertification since 1970s due to overgrazing, excessive reclamation, and the over-gathering of fuel wood under the pressure of fast increases in the local population, and over 34% of the total land area has been desertified [15]. Revegetation on mobile sand land under the protection of straw checkerboards was commonly adopted to control grassland desertification since the 1980s. Thus far, large areas of sand-fixation plantations of indigenous trees, shrubs, and grasses have been established in this region, which has resulted in significant improvement in the local environment. According to field investigation, the afforestation on mobile or semi-mobile sand dunes facilitated the formation and development of BSC. Physical crusts can be firstly formed by the translocation and deposition of fine particles in the initial phase during the stabilization of a mobile sand dune, and subsequently gradually evolve into BSC due to increases in the population of fungi, cyanobacteria, and nonvascular plants (lichens and mosses). Bacteria and fungi are the most basic components in physical crusts and BSCs, which play important roles in soil carbon (C), nitrogen (N), and phosphorus (P) cycles and soil fertility improvement, thereby affecting the development of herbaceous plant communities in a given plantation [1,5,16]. The responses of microbial functional taxa involved in the N cycle and P transformation to BSC succession were investigated in this area [5,7], which provides some useful information for understanding the microbiological mechanisms behind the bio-availabilities of the nutrients of BSCs. However, the studies on the dynamics of the composition and structure of microbial communities along BSC succession are still insufficient. The response patterns of dominant microbial taxa to BSC succession and the main factors driving microbial community succession should be studied to further understand the ecological function of BSC, artificially facilitate the development of BSC, and accelerate the succession process of herbaceous plant communities in sand-fixation plantations.
In this study, we investigated how a chronosequence of BSCs in the Horqin sand land differed in edaphic attributes and the structures of bacterial and fungal communities. The objectives of this study were to (1) determine the dynamics of the structures of microbial communities across BSC development, and (2) examine the interactions between soil attributes and microbial communities. We assumed that the microbial diversities would increase along BSC succession and the improved soil nutrient status would alter the structures of the microbial communities. The results are expected to provide some novel ideas for how to accelerate BSC succession in sand-fixation plantations by regulating the structures of microbial communities via soil improvement.

2. Materials and Methods

2.1. Study Location and Site Description

This study was conducted at the experimental demonstration area for desertification control of Wulanaodu Desertification Combating Ecological Station under the Institute of Applied Ecology, Chinese Academy of Sciences, in western Horqin Sandy Land (43°02′ N, 119°39′ E, 479 m a.s.l.). Wulanaodu is located in the semi-arid region of the north temperate zone, characterized as a landscape mosaic of mobile/semi-mobile sand dunes, fixed sand dunes, wind-eroded grassland, and interdune lowland. It has a semi-arid continental monsoon climate with four distinct seasons and an average temperature of 6.3 °C. The annual mean precipitation and pan evaporation are 340 mm and 2500 mm, respectively. The soils were classified as Cambic Arenosols [17]. The original vegetation belongs to the transitional type from forest to grassland represented by Ulmus pumila L. open forest. However, most of the dominant original species has been gradually replaced by psammophytes in recent decades due to the serious desertification induced by overgrazing, over-reclamation, and heavy plant harvesting. At present, the dominant native plants include Pennisetum flaccidum Griseb., Caragana microphylla Lam., Bassia dasyphylla O. Kuntze, Artemisia halodendron Turcz., Chenopodium acuminatum Willd., and Salix gordejevii Chang et Skv. To fix mobile/semi-mobile sand dunes, some native shrubs (e.g., C. microphylla and S. gordejevii) were commonly planted under the protection of grass-checked sand barrier (usually made of straw and 1 m × 1 m squares), which was conducive to reducing the wind velocity, stabilizing the sand surface, and improving the survival rates of seedlings. After 3–5 years, sand-fixation plant communities gradually formed and the sand dunes were completely fixed, which subsequently accelerated the development of BSCs on the surface soil. Since the 1980s, a large area of sand-fixing plantations has been established in the experimental demonstration area around Wulanaodu region.

2.2. Soil Sampling

An age sequence of C. microphylla plantations (10-, 22-, and 37-year-old) and their adjacent moving sand dunes (designated as SC10, SC22, SC37, and MSD, respectively) were selected as experimental sites. C. microphylla is a native leguminous shrub, widely used to stabilize the moving and semi-moving sand dunes in this region. The plantations were all established on MSDs at different times; therefore, MSDs can be considered as experimental controls. Three sites of SC10, SC22, SC37, and MSD were set up at different sand dunes for sampling. Each site was over 300 m away from the others. For each plantation site, one 30 m × 30 m plot was established, and ten representative C. microphylla clumps were selected. Under the crown of each clump, subsamples of BSC were collected from four directions. Similarly, 0–1 cm topsoil sample in each MSD site was randomly collected. Half of each sample was air-dried, and the other half was frozen at −80 °C in a refrigerator.

2.3. Determination of Soil Properties

The soil pH was measured in soil–water suspensions (1:2.5). The soil organic matter and total N were determined using the K2Cr2O7–H2SO4 oxidation and the semimicro-Kjeldahl digestion methods, respectively. The soil total P and available P were measured using the acid-digestion molybdate colorimetric method and the molybdate ascorbic acid method (in 0.5 M NaHCO3), respectively. The total K and available K were measured using the atomic absorption spectroscopy method. Fresh soils were extracted with 1 M KCl solution, and then NH4-N in filtering solution was measured using an automated discrete analyzer (CleverChem 380, Hambeug, Germany). The soil moisture was determined by a drying method. The experimental procedures of the above indicators all followed the descriptions in the ISSCAS [18].
Soil protease activity was measured using the method of Ladd and Bulter [19]. The activities of urease and polyphenol oxidase (POA) were determined according to the methods described by Kandeler and Gerber [20] and Perucci et al. [21], respectively. Alkaline phosphomonoesterase (ALP) activity was measured according to the procedure of Tabatabai [22]. The activities of nitrate reductase and dehydrogenase were determined using the method of Schinner et al. [23] and the ISSCAS [24], respectively. The measurement procedures of the soil enzymatic activities are described in the Supplementary Materials and Methods.

2.4. DNA Extraction, 16S rDNA and Internal Transcribed Spacer (ITS) rDNA Sequencing, and Data Processing and Analysis

Microbial DNA was extracted from 0.3 g fresh soil sample by using the FastDNA Spin Kit (Tiangen Biotech, Beijing, China). Next generation sequencing library preparations and Illumina MiSeq sequencing were conducted at GENEWIZ, Inc. (Suzhou, China). The V3 and the V4 regions of the bacterial 16S rRNA genes and fungal ITS2 region genes were amplified. The primers, the clustering of operational taxonomic units (OTUs), the OTU richness analysis, and hierarchical clustering analysis are described in the Supplementary Materials and Methods. The OTUs were taxonomically classified using the Ribosomal Database Program (RDP) classifier [25]. The classification of bacteria and fungi was according to the taxonomy systems of Bergey and Kirk et al. [26], respectively. Raw sequencing datasets were deposited in the NCBI Sequence Read Archive under the accession number PRJNA942069.

2.5. Regression Analysis and Redundancy Analysis (RDA)

The responses of the soil properties, dominant taxa, and alpha diversity indexes of the microbial communities to BSC age were evaluated using the linear regression model performed using the SPSS 13.0 software package (SPSS Co., Ltd., Chicago, IL, USA). The Pearson correlations between soil properties and the relative abundances of dominant bacterial/fungal genera as well as alpha diversity indexes were calculated. p < 0.05 was considered as statistically significant. Redundancy analysis (RDA) between the soil properties and the structure of bacterial/fungal communities was performed using CANOCO 5.0 software (Biometris-Plant Research International, Wageningen, The Netherlands), and the correlations of the soil properties were examined by a Monte Carlo permutation.

3. Results

3.1. Soil Property Improvement along BSC Development

The values of the soil moisture (SM), pH, organic matter (SOM), total N (TN), total P (TP), total K (TK), NH4-N, available P (AP), and available K (AK), as well as their changing trends along BSC development, are listed in Table 1. Except for TK, all the selected soil physicochemical properties significantly increased with BSC age. SOM, pH, SM, TN, TP, NH4-N, AP, and AK in SC10, SC22, and SC37, sites were 4.8–12.2, 1.0–1.1, 2.7–4.3, 1.1–1.4, 1.6–2.1, 9.1–12.6, 8.6–14.3, and 3.7–5.0 times higher than that in MSD, respectively. Significant linear relationships between BSC age and SOM, pH, SM, TN, TP, NH4-N, AP, and AK were found, respectively (p < 0.01, R2 = 0.535 to 0.932). However, no significant differences in TK among different sites were found. Similarly, the activities of the selected three soil hydrolases (including phosphomonoesterase, urease, and protease) and three oxidoreductases (including dehydrogenase, polyphenol oxidase, and nitrate reductase) also significantly linearly increased across the development of BSC (R2 = 0.657 to 0.928, p ≤ 0.001). The activities of phosphomonoesterase, urease, protease, dehydrogenase, polyphenol oxidase, and nitrate reductase in BSC sites were 25.9–71.6, 13.8–31.1, 18.4–40.1, 3.8–11.9, 2.1–3.0, and 281.2–291.3 times higher than that in MSD sites, respectively. The increasing rates of enzymatic activities across BSC development were faster than those of soil nutrients. The results confirmed that the afforestation of native shrubs on shifting sand dunes can ameliorate the microenvironment, nutrient content, and microbiological properties of BSC on the surface soil.

3.2. Response of Soil Bacterial Community to BSC Development

Extracted microbial DNA from twelve samples was sequenced using an Illumina MiSeq high-throughput sequencing platform. After controlling for quality, a total of 622,588 16S rDNA sequences 446–452 bp in length were obtained and 1090 OTUs were clustered. The abundance-based coverage estimator (ACE), Shannon–Wiener index (SW), observed OTUs, and Chao’s species richness estimator (Chao) were calculated based on the clustered OTUs, and the results are listed in Table 2. The ACE, SW, observed OTUs, and Chao of the BSC sites were 1.5–1.7, 1.1–1.2, 1.6–1.9, and 1.6–1.8 times larger than that of MSD sites, respectively, and they all exhibited significantly linearly increasing tendencies across BSC age (Table 2, R2 = 0.643 to 0.691; p < 0.01). Hierarchical clustering analysis grouped 12 samples into four clusters. The three samples from the BSC sites of the same age or MSD were individually grouped into one cluster, indicating the differentiation in soil bacterial community structures among different sites (Figure 1a). The calculated Pearson coefficient indicated that the observed OTUs, ACE, Chao, and SW were significantly positively correlated with soil attributes (except for TK and SW to NH4-N) (p < 0.05, Table 3).
All the detected 16S rDNA sequences were classified into 24 phyla, 58 classes, 77 orders, 122 families, or 143 genera. The dominant bacterial phyla (average relative abundance > 1%) included Proteobacteria (27.5%), Actinobacteria (15.7%), Acidobacteria (13.8%), Bacteroidetes (13.8%), Cyanobacteria (11.9%), Chloroflexi (8.8%), Firmicutes (3.1%), and Gemmatimonadetes (2.3%). The dynamic patterns of the relative abundances of phyla across BSC development are described in Figure 2a. The changes in the abundances of dominant phyla along BSC development varied with phylum type. Proteobacteria and Bacteroidetes significantly linearly increased across BSC age, while Actinobacteria and Chloroflexi significantly linearly decreased (Figure 3, p < 0.01). The relatively abundances of Cyanobacteria and Acidobacteria in BSC sites increased 35.8–87.6 and 1.1–2.1 times compared to MSD, while that of Firmicutes significantly decreased.
At the generic level, eighteen dominant genera with relative abundances ≥1% in MSD or BSC sites were detected, i.e., Sphingomonas, RB41, Ambiguous, Microcoleus, Segetibacter, Bacillus, Blastocatella, Flavisolibacter, Flavobacterium, Microvirga, Haliangium, Pseudarthrobacter, Roseiflexus, Bryobacter, Gaiella, Rubellimicrobium, Solirubrobacter, and Streptomyces (Figure 2b). As a whole, the generic composition of the bacterial community in MSD was significantly different from that in the BSCs. Sphingomonas, RB41, and Microcoleus were the most abundant genera in the BSC sites (>5.0%), while the most abundant genera in the MSD sites were Ambiguous, Bacillus, Gaiella, and Pseudarthrobacter, with the average relative abundances of 10.7%, 9.4%, 3.1%, and 2.2%, respectively. The observed 53 genera in the BSC sites were not detected in the MSD; meanwhile, 12 genera detected in the MSD were absent in the BSC sites. The remaining genera were the common compositions in the MSD and BSC sites, but varied in their relative abundances. Additionally, the waxing and waning responses of some dominant genera to BSC development were found. Sphingomonas, RB41, Segetibacter, Flavisolibacter, and Haliangium significantly linearly increased across BSC age (p < 0.05), while Ambiguous, Pseudarthrobacter, and Roseiflexus linearly decreased (Figure 4; p < 0.05). This phenomenon suggested that these dominant genera were sensitive to BSC development and might play important roles during bacterial community succession.

3.3. Response of Soil Fungal Community to BSC Development

A total of 944,675 ITS sequences with 302–336 bp in length were obtained, and 667 OTUs were identified. Except for the SW, significant differences in the observed OTUs, Chao, and ACE indexes among different sites were observed (Table 2). Similar to the bacterial community, significantly linearly increasing tendencies of observed OTUs, Chao, and ACE across BSC development were also found (Table 2, p ≤ 0.01). Significantly positive correlations between alpha diversity indexes (except for the SW) and soil properties (except for TK) were also observed (p < 0.05, Table 3). All the samples were also clustered in four groups by hierarchical clustering analysis, clearly showing the significant difference in fungal community structure between different sites (Figure 1b).
The relative abundances are expressed by color intensity: a: bacterial phylum; b: bacterial genus; c: fungal phylum; and d: fungal genus. MSD means moving sand dune, and SC-10, SC-22, and SC-37 refer to 10-, 22-, and 37-year biological soil crust, respectively.
The clustered fungal OTUs were classified into 4 phyla, 15 class, 40 orders, 58 families, 91 genera, or 132 species. Ascomycota was the absolutely dominant phylum in all the samples (60.7% to 79.9%), followed by Basidiomycota (4.2% to 14.8%, Figure 2c). No significant differences in the relative abundances of fugal phyla between the different sites were observed. At the generic level, seventeen dominant fungal genera with relative abundances ≥ 1% in the MSD and BSC sites were detected. In the MSD sites, the dominant genera included Gloeotinia (with the average relative abundance of 28.9%), Emericella (6.6%), Saccharomyces (6.0%), Phialemonium (5.4%), Rhizopus (5.1%), Malassezia (5.0%), Aureobasidium (4.4%), Candida (3.0%), Alternaria (1.6%), and Valsa (1.6%); while Mycocentrospora (15.2%), Myrothecium (11.2%), Coniothyrium (7.8%), Fusarium (2.7%), Alternaria (2.3%), Athelia (2.6%), and Bovista (2.1%) were more abundant in the BSC sites. Only 30 fungal genera were observed in the MSD sites, while 78 genera were detected in the BSC sites. Furthermore, 61 genera observed in the BSC sites were absent in the MSD sites, and 15 genera detected in the MSD sites were absent in the BSCs. The remaining genera were found both in MSD and BSC sites, but varied in their relative abundances. The varying patterns of the relative abundances of the dominant genera are described in Figure 2d. Therefore, the formation of BSC on the surface of the MSDs significantly altered the fungal generic composition, richness, and community structure. Although most OTUs cannot be identified at the species level, obvious dynamic changes in the relative abundances of some observed dominant species were still found during BSC development. For example, Gloeotinia temulenta (28.9%) was the absolutely dominant species in the MSD sites, while its relative abundance dramatically decreased to <0.01% in the BSC sites; the other four dominant species, including Emericella nidulans (6.6%), Rhizopus oryzae (5.1%), Malassezia restricta (4.0%), and Candida parapsilosis (3.0%), disappeared in the BSC sites. Simultaneously, Coniothyrium aleuritis (7.8%), Alternaria brassicae (2.2%), and Athelia pyriformis (2.6%) gradually evolved into the dominant species. These results indicated that the formation of BSC under the plantations increased soil fungal diversity and changed the community structure, and the community succession was characterized by the quantitative alternation of dominant taxa and the gradual invasions of some new taxa.

3.4. Dependence of Bacterial and Fungal Community Structures on Soil Variables

RDA was performed to analyze the relationships between the structures of bacterial and fungal communities and soil properties. Figure 5 indicated that 61.7% and 69.0% of variations in bacterial and fungal community structures can be explained in the first axis, and 17.6% and 14.9% in the second axis, respectively. RDA also clustered the total samples into four groups, which were nearly consistent with the result of hierarchical clustering analysis (Figure 1), indicating the structural differentiation of microbial communities along BSC development. According to the Monte Carlo permutation test, the selected soil variables (except for TK) all significantly positively affected the structural variations of bacterial and fungal communities (Figure 5, p < 0.05). Additionally, the Pearson correlations between soil factors including enzymatic activities and the relative abundances of some dominant genera were also calculated (Table S1). Table S1 shows that the responses of dominant genera to soil property improvement varied with generic type and soil factors. Some bacteria (e.g., Sphingomonas, Ambiguous, Segetibacter, and Pseudarthrobacter) and fungi (Gloeotinia, Emericella, Saccharomyces, and Aureobasidium) were more sensitive to soil property variations than the other genera. Most dominant bacterial genera significantly correlated to soil available nutrients (NH4-N, AP, and AK), while SM, NH4-N, nitrate reductase, and polyphenol oxidase widely correlated to most dominant fungal genera (Table S1). However, some bacteria and fungi were not affected by soil environmental change, which were intrinsic members of their microbial communities and might make important contributions to the reformation and succession of their microbial communities.

4. Discussion

Soil crust is a special ecological interface connecting the atmosphere and soil in desertification regions, which plays important roles in maintaining the stability of surface soil, regulating water distribution, accumulating soil nutrients, and conserving microbial diversity [6,12,27]. Its positive contributions to reversing desertification are also well documented [1,4,10,28]. However, the response of microbial communities in BSC to revegetation in desertified land is not well understood. The present study investigated the bacterial and fungal diversities and structural dynamics of microbial communities of BSC to further describe the effect of ecological restoration using native shrub plantation on mobile sand lands.

4.1. The Formation of BSC and Soil Property Improvement

The moving sand dunes (MSDs) in Horqin Sandy Land were gradually formed under long-term wind erosion and sand deposit. Physical soil crusts can be widely observed on the surface of MSDs especially in summer and autumn; however, biological soil crusts (BSCs) cannot be naturally formed because of the instability of MSDs and intense wind erosion in spring and winter. The afforestation of native shrubs on MSDs can facilitate the formation of BSC [10], which is a complex ecological process influenced by many factors simultaneously. Sand-fixation plantation can stabilize sand dunes, reduce wind velocity, improve the microenvironment, alter the albedo water–heat balance of the underlying surface, and intercept and deposit fine soil particles [29,30]. Additionally, rapid increases in shrub litter and the death of herbaceous plants also contribute to soil nutrient improvement, and especially SOM. All these effects are favorable to the formation of BSC. The increase in soil N mainly depends on the N-fixation by Azotobacter, which are symbiotic with leguminous plants, and the N-release from litter decomposition [3,16]. The amelioration of soil nutrients is bound to increase the quantity of microorganisms, which are the essential components of BSC. This study showed that soil moisture, pH, and nutrients (including SOM, TN, TP, NH4-N, AP, and AK) in BSC were all much higher than that in MSDs, and all presented linearly increasing tendencies along BSC development (Table 1), indicating that BSC had significant effects on improving the microenvironment and accumulating soil nutrients. However, no significant change in soil TK among different sites was observed. The parent material of sandy soil is relatively rich in K (generally > 2%), which can basically meet the demand for plant growth [31]. Therefore, it is generally considered that TK is not a key factor affecting plant growth and soil quality in this sandy land. The improvement of soil nutrients is the prerequisite and foundation for increases in microbial quantity and the succession of a given microbial community [5].
The activities of protease, urease, phosphomonoesterase, dehydrogenase, polyphenol oxidase, and nitrate reductase presented similar varying tendencies to soil nutrients (Table 1), suggesting an improvement in soil redox rate and an increase in the quantity of microorganisms associated with N and P transformation [5,32], because most soil enzymes are secreted by microorganisms. The main factors affecting these enzymatic activities in sandy land are soil nutrients and O2 availability, because they are determinants of soil microbial growth [33]. The increased activities of soil urease, protease, and phosphomonoesterase can accelerate the mineralization rate of N- or P-containing organic compounds in soil. Simultaneously, increases in the activities of dehydrogenase, nitrate reductase, and polyphenol oxidase can improve soil redox condition and the chemical properties of soil solution, which is conducive to the bond dissociation between metals and complex organic matter, thereby improving the bioavailability of N and P in soil. This study also found that soil enzyme activities increased at much higher rates than soil nutrients during BSC development. This phenomenon suggests that on a small scale, soil enzymes are more sensitive to environmental variations than other soil variables, and can be used as indicators monitoring soil quality and microbiological activity [34].

4.2. Recovery and Succession of Soil Bacterial/Fungal Community in BSC

Revegetation on MSDs can induce the formation of BSC and significantly influence the microbial community through complicated processes, including changes in the microenvironment, production of litter, rhizodeposition, secretion of root exudates, and interactions with root-symbiotic organisms [35,36]. MSD fixation and the improvement of soil fertility directly contributed to the increases in microbial quantity and diversity of BSC. In this study, the observed OTUs, Chao, and ACE indices of bacterial and fungal communities in BSC were all significantly higher than that in MSDs, showing the similar linearly increasing tendencies to soil nutrients and enzymatic activities (Table 1 and Table 2). The results suggested that BSC formation promoted the gradual recovery of microbial community and the increases in bacterial and fungal diversities. Plant–soil-microbe interactions significantly influence the reformation and structure dynamic of microbial communities, which can lead to many variations in ecological processes including litter decomposing, N-fixation, and P-mineralization, thus increasing soil total and available nutrients [37].
Proteobacteria, Actinobacteria, Acidobacteria, Bacteroidetes, Cyanobacteria, Chloroflexi, Firmicutes, and Gemmatimonadetes were detected in the MSD and BSC sites, which were similar to some oligotrophic habitats [38,39,40]. Simultaneously, three dominant fungal phyla, i.e., Ascomycota, Basidiomycota, and Zoopagomycota, were found in the MSD and BSC sites. The three fungal phyla were also observed in black soil and fluvo-aquic soil in the Northeast China Plain, and fertilization regime significantly affected their relative abundances [35]. Delgado et al. [41] also reported that Ascomycota and Basidiomycota dominated the soil fungal community under the low montane humid forest and their relative abundances varied with soil types. In this study, the response of dominant taxa to BSC development varied with sites, and their relative abundances showed the waning and waxing characteristic (Figure 2, Figure 3 and Figure 4). Our results indicated that the microbial community structure in BSCs was significantly different from that in MSD. In other words, the formation of BSC on MSDs co-occurred with the progressive successions of microbial communities, presenting an interactive relationship. Although the relative abundances were different, the basic compositions, especially of the dominant microbial taxa, among the different age BSC sites were similar. The above results suggest that the succession of a the microbial community of the BSC was characterized by a sequential process including an initial phase of faster recoveries of dominant taxa, a subsequent slower development phase, and a final stable phase (Figure 1), which was similar to the secondary succession process of the plant community.
MSD is not a favorable habitat for microbes due to its unstable, severely arid, and oligotrophic environment, though some species with high capacities to utilize limited nutrients can survive in MSDs. During the formation of an MSD, the gradually deteriorated habitat generally leads to the disappearance and/or the predominance of some taxa because of interspecific competition. Therefore, less taxa and lower diversities of bacteria and fungi were observed in MSDs in this study. Revegetation on MSDs improved the microenvironment, induced the formation of BSC, and resulted in the increase in microbial quantity. The soil microbial community was gradually restored, which was characterized by the re-invasion of taxa that had disappeared and alternations in the relative abundances of dominant taxa (Figure 2). The recovery of a soil microbial community inevitably leads to a shift in soil microbiological functions. Zhao et al. [5] reported BSC development increased the soil P transformation rate based on increases in the quantity and diversity of phoD- and gcd-harboring microbes. The diversities of N cycle-related microbes including nitrogen-fixing, ammonia-oxidizing, and denitrifying bacteria also significantly increased along sand-fixation plantation development [7]. Consistent with Jangid et al. [42] and Suleiman et al. [43], some resilient core microbial taxa unrelated to soil properties were found both in MSD and BSC sites, which were basic components of the microbial community and might have served important functions in the reformation, succession, and maintaining stability of the soil microbial community.
The successions of microbial communities are primarily directly driven by soil and vegetation, because they provide the essential microenvironment and nutrition for microbial survival [44]. Our results also confirmed that the differentiation in microbial community structures among the different sites was directly affected by soil pH, SM, and nutrients. Most dominant bacterial genera significantly correlated with NH4-N, AP, and AK, and most dominant fungal genera were significantly correlated with SM, NH4-N, nitrate reductase, and polyphenol oxidase. Shifts in the abundances of dominant taxa are the significant characteristic of microbial community succession [45]. Therefore, SM, available nutrients, nitrate reductase, and polyphenol oxidase were considered the dominant factors driving microbial community succession in BSC within the studied continuous landscape.

5. Conclusions

The formation of BSC facilitated the improvement of the microenvironment, the accumulation of soil nutrients, and increases in enzymatic activities (phosphomonoesterase, urease, protease, dehydrogenase, polyphenol oxidase, and nitrate reductase). Soil nutrients and enzymatic activities all linearly increased with BSC age, and soil enzymes were more sensitive to BSC development than soil nutrients. Soil bacterial and fungal communities can be gradually restored on MSDs depending on the formation and development of BSC. The diversities of soil microbial communities increased across BSC development. Significant differences in the structures of the microbial communities of the MSDs and early stage BSC were observed, and similar microbial compositions among the different BSC sites were found. The successions of the microbial communities in BSC were characterized by a sequential process including an initial phase of faster recoveries of dominant taxa, a subsequent slower development phase, and a final stable phase. The quantitative responses of the dominant microbial taxa to BSC development varied by dominant taxa, showing the waning and waxing characteristic. The secondary successions of the microbial communities of the BSC were directly driven by soil factors, and SM, available nutrients, nitrate reductase, and polyphenol oxidase were the main influencing factors.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f15091631/s1, File S1: Supplementary Materials and Methods; Table S1: Correlations between the relative abundance of dominant bacterial/fungal genera and soil properties.

Author Contributions

C.C.: writing—original draft, data curation, reviewing and editing, conceptualization, and project administration; Y.Z.: writing—original draft and methodology; Z.C.: resources and investigation. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded the National Natural Science foundation of China (42277467, 41877536).

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Materials; further inquiries can be directed to the corresponding author(s).

Acknowledgments

The authors would like to express their gratitude to the Wulanaodu Desertification Combating Ecological Station under the Institute of Applied Ecology, Chinese Academy of Sciences.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Cluster analysis of the structures of soil bacterial (a) and fungal (b) communities. MSD: moving sand dune; SC-10, SC-22, and SC-37: 10-, 22-, and 37-year biological soil crust, respectively.
Figure 1. Cluster analysis of the structures of soil bacterial (a) and fungal (b) communities. MSD: moving sand dune; SC-10, SC-22, and SC-37: 10-, 22-, and 37-year biological soil crust, respectively.
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Figure 2. Relative abundances of dominant taxa in different sites. (a): bacterial phylum; (b): bacterial genus; (c): fungal phylum; (d): fungal genus. MSD: moving sand dune; SC-10, SC-22, and SC-37: 10-, 22-, and 37-year biological soil crust, respectively.
Figure 2. Relative abundances of dominant taxa in different sites. (a): bacterial phylum; (b): bacterial genus; (c): fungal phylum; (d): fungal genus. MSD: moving sand dune; SC-10, SC-22, and SC-37: 10-, 22-, and 37-year biological soil crust, respectively.
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Figure 3. Linear responses of the relative abundances of dominant bacterial phyla to biological soil crust age. (a): Proteobacteria; (b): Actinobacteria; (c): Chloroflexi; (d): Bacteroidetes.
Figure 3. Linear responses of the relative abundances of dominant bacterial phyla to biological soil crust age. (a): Proteobacteria; (b): Actinobacteria; (c): Chloroflexi; (d): Bacteroidetes.
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Figure 4. Linear responses of the relative abundances of dominant bacterial genera to BSC age. (a): Sphingomonas; (b): RB41; (c): Ambiguous; (d): Segetibacter; (e): Flavisolibacter; (f): Haliangium; (g): Pseudarthrobacter; (h): Roseiflexus.
Figure 4. Linear responses of the relative abundances of dominant bacterial genera to BSC age. (a): Sphingomonas; (b): RB41; (c): Ambiguous; (d): Segetibacter; (e): Flavisolibacter; (f): Haliangium; (g): Pseudarthrobacter; (h): Roseiflexus.
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Figure 5. RDA between bacterial (a)/fungal (b) community structure and soil properties. SM: soil moisture; SOM: soil organic matter; TN: total N; AN: NH4-N; TP: total P; AP: available P; AK: available K. MSD: moving sand dune (0 yr); SC10, SC22, and SC37: 10, 22, and 37 yr biological soil crust, respectively.
Figure 5. RDA between bacterial (a)/fungal (b) community structure and soil properties. SM: soil moisture; SOM: soil organic matter; TN: total N; AN: NH4-N; TP: total P; AP: available P; AK: available K. MSD: moving sand dune (0 yr); SC10, SC22, and SC37: 10, 22, and 37 yr biological soil crust, respectively.
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Table 1. Soil properties and enzymatic activities in the chronosequence of BSCs.
Table 1. Soil properties and enzymatic activities in the chronosequence of BSCs.
IndexMSDSC10SC22SC37ANOVA in Response to Age
Regress EquationR2Fp
Soil moisture (%)0.25 ± 0.090.69 ± 0.150.87 ± 0.081.09 ± 0.146y = 0.021x+ 0.3580.83550.55<0.001
pH6.64 ± 0.136.81 ± 0.066.93 ± 0.087.03 ± 0.05y = 0.010x + 6.6760.78336.02<0.001
Soil organic matter (%)0.09 ± 0.010.43 ± 0.110.83 ± 0.101.10 ± 0.15y = 0.027x + 0.1390.932136.1<0.001
Total N (%)0.018 ± 0.0010.019 ± 0.0020.022 ± 0.0020.026 ± 0.003y = 0.001x + 0.0070.73127.21<0.001
Total P (%)0.041 ± 0.0010.022 ± 0.0010.024 ± 0.0040.029 ± 0.006y = 0.001x + 0.0160.73327.51<0.001
Total K (%)2.24 ± 0.102.25 ± 0.122.23 ± 0.112.33 ± 0.11-0.0911.0060.340
NH4-N (mg kg−1)1.50 ± 0.0713.5 ± 0.7318.9 ± 1.5215.2 ± 1.08y = 0.348x + 6.2720.53511.510.007
Available P (mg kg−1)0.55 ± 0.154.66 ± 0.796.82 ± 0.457.77 ± 0.93y = 0.187x + 1.7230.83249.36<0.001
Available K (mg kg−1)43.8 ± 3.18161.7 ± 4.68178.3 ± 10.5220.4 ± 13.1y = 4.288x + 77.070.80841.96<0.001
Nitrate reductase (μg g−1)0.006 ± 0.0021.69 ± 0.141.64 ± 0.371.75 ± 0.10y = 0.042x + 0.4680.65719.140.001
ALP (mg g−1 h−1)5.70 ± 2.75147.4 ± 35.9241.9 ± 85.8408.0 ± 21.6y = 10.54x + 18.910.925123.4<0.001
POA (μmol g−1 10 min−1)0.34 ± 0.040.72 ± 0.180.80 ± 0.181.02 ± 0.15y = 0.017x + 0.4300.72426.22<0.001
Dehydrogenase (mg kg−1)48.1 ± 1.58183.3 ± 57.5332.9 ± 63.4572.4 ± 97.0y = 14.065x + 41.550.928129.7<0.001
Protease (μg g−1 2 h−1)4.89 ± 3.7289.8 ± 51.7133.5 ± 8.1196.0 ± 26.7y = 4.942x + 20.7930.86262.34<0.001
Urease (mg g−1 24 h−1)0.11 ± 0.011.52 ± 0.472.5 ± 0.423.42 ± 0.31y = 0.087x + 0.3810.914106.2<0.001
Values are means ± SD (n = 3). MSD: moving sand dune (0 yr); SC10, SC22, and SC37: 10, 22, and 37 yr biological soil crust, respectively; ALP: alkaline phosphomonoesterase; POA: polyphenol oxidase. R2, F, and p values from regression analysis are given.
Table 2. Alpha diversity indexes of soil bacterial and fungal communities in different soil crusts.
Table 2. Alpha diversity indexes of soil bacterial and fungal communities in different soil crusts.
IndexMSDSC10SC22SC37R2p
Observed OTUsBacteria398 ± 34 a650 ± 68 b691 ± 40 b736 ± 17 b0.6910.001
Fungi49 ± 26 a329 ± 18 b346 ± 56 b372 ± 14 b0.6130.003
ACEBacteria466.6 ± 81.6 a720.7 ± 62.7 b761.1 ± 792.3 b792.3 ± 14.8 b0.6350.002
Fungi55.1 ± 27.2 a346.3 ± 14.0 b371.9 ± 46.8 bc415.0 ± 18.3 c0.6690.001
Chao1 estimatorBacteria469.2 ± 85.7 a729.5 ± 62.6 b771.5 ± 20.0 b805.3 ± 14.7 b0.6430.002
Fungi51.5 ± 26.1 a349.5 ± 11.7 b370.1 ± 45.0 bc416.9 ± 20.0 c0.6660.010
Shannon–WienerBacteria6.903 ± 0.336 a7.239 ± 0.533 b7.428 ± 0.163 b7.975 ± 0.059 b0.6650.001
Fungi3.828 ± 0.478 a5.343 ± 0.636 a4.677 ± 1.030 a5.121 ± 0.262 a0.1800.170
MSD: moving sand dune (0 yr); SC10, SC22, and SC37: 10, 22, and 37 yr biological soil crust, respectively. A total of 20,665 and 45,523 randomly sampled sequences were used for bacterial and fungal diversity estimates, respectively. Means in rows followed by different letters are significantly different (p < 0.05) based on one-way ANOVA followed by the LSD test. The R2 and p values from linear regression analysis are given.
Table 3. Correlations between alpha diversity indexes and soil properties (n = 12).
Table 3. Correlations between alpha diversity indexes and soil properties (n = 12).
Index SMpHSOMTNTPTKNH4-NAPAK
Observed OTUsBacteria0.907 **0.857 **0.851 **0.941 **0.794 **0.2740.909 **0.950 **0.951 **
Fungi0.878 **0.810 **0.806 **0.953 **0.784 **0.1730.934 **0.924 *0.948 **
ACEBacteria0.892 **0.858 *0.821 **0.929 **0.772 **0.2780.901 **0.925 **0.924 **
Fungi0.900 **0.833 **0.834 **0.968 **0.806 **0.1810.934 **0.939 **0.963 **
Chao1 estimatorBacteria0.896 **0.857 *0.826 **0.933 **0.778 **0.2640.900 **0.926 **0.926 **
Fungi0.903 **0.828 **0.830 **0.968 **0.797 **0.1950.931 **0.934 **0.963 **
Shannon–WienerBacteria0.823 **0.626 *0.789 **0.662 *0.646 *0.1120.5490.730 **0.739 **
Fungi0.5460.4990.4400.581 *0.4090.4280.5200.5570.611 *
SM: soil moisture; SOM: soil organic matter; TN: total N; TP: total P; TK: total K; AP: available P; AK: available K. * p < 0.05; ** p < 0.01.
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Cao, C.; Zhang, Y.; Cui, Z. Successions of Bacterial and Fungal Communities in Biological Soil Crust under Sand-Fixation Plantation in Horqin Sandy Land, Northeast China. Forests 2024, 15, 1631. https://doi.org/10.3390/f15091631

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Cao C, Zhang Y, Cui Z. Successions of Bacterial and Fungal Communities in Biological Soil Crust under Sand-Fixation Plantation in Horqin Sandy Land, Northeast China. Forests. 2024; 15(9):1631. https://doi.org/10.3390/f15091631

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Cao, Chengyou, Ying Zhang, and Zhenbo Cui. 2024. "Successions of Bacterial and Fungal Communities in Biological Soil Crust under Sand-Fixation Plantation in Horqin Sandy Land, Northeast China" Forests 15, no. 9: 1631. https://doi.org/10.3390/f15091631

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