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Article

Differential Effects of Organic Ameliorants on the Reassembly of Bacterial Communities in Newly Amended Coastal Mudflat Salt-Affected Soil

by
Yunlong Li
1,2,
Yimin Wang
1,
Chuanhui Gu
3,
Chao Shen
1,
Lu Xu
1,
Yilin Zhao
1,
Siqiang Yi
1,
Wengang Zuo
1,2,
Yuhua Shan
1,2,4,
Zhuqing Zhang
5,* and
Yanchao Bai
1,2,4,*
1
College of Environmental Science and Engineering, Yangzhou University, Yangzhou 225127, China
2
Key Laboratory of Arable Land Quality Monitoring and Evaluation, Key Laboratory of Saline-Alkali Soil Improvement and Utilization (Coastal Saline-Alkali Lands), Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou 225127, China
3
Environmental Research Center, Duke Kunshan University, Kunshan 215316, China
4
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing 210095, China
5
College of Chemistry and Environmental Engineering, Yangtze University, Jingzhou 434022, China
*
Authors to whom correspondence should be addressed.
Agronomy 2022, 12(10), 2525; https://doi.org/10.3390/agronomy12102525
Submission received: 6 September 2022 / Revised: 7 October 2022 / Accepted: 13 October 2022 / Published: 16 October 2022
(This article belongs to the Special Issue Effects of Organic Amendments on Soil Carbon Storage and Food Production)
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Abstract

:
Understanding the influences of organic ameliorants amendment on the soil microbiome is fundamental for the alleviation of environmental constraints in coastal mudflat salt-affected soils. However, how the compositional and structural diversity of the microbial community responds to different organic inputs, and key environmental determinants and relevant mechanisms driving soil microbiome reassembly in coastal agroecosystems have not been illustrated. In this study, field experiments were conducted to investigate the effectiveness and underlying mechanisms of sewage sludge (S) and sludge-based vermicompost (V) at different application amounts (0, 50, 100, and 200 t ha−1) on variations in the compositional and structural diversities of soil bacterial community in coastal mudflats. The underlying driving factors, including soil physicochemical and enzymatic properties, were determined to estimate their effects on soil bacterial community. Results show that both types and amounts of organic ameliorants exerted significant influence on the alterations of bacterial community diversities. Particularly, restructured bacterial communities with significantly higher bacterial populations, lower Shannon diversities, and distinct core and unique community profiles were observed in organic ameliorant-amended soils as compared to CK. The co-occurrence networks of bacterial core OTUs reveal that V exhibited more profound effects than those of S on the scale and interactions enhancement and stability reduction of soil bacterial guilds. Additionally, both S and V significantly alleviated environmental constraints with lower pH and salinity, but higher soil organic carbon (SOC) amounts and enzyme activities were observed in the amended soils. Moreover, the effects of S and V on soil amendment were enhanced with the increase in the application amounts of organic ameliorants. Redundancy analysis (RDA) reveals that environmental factors (e.g., pH, salinity, SOC, sucrase, urease, and phosphatase) were pivotal determinants, accounting for 78.05% of the total bacterial community variations in coastal salt-affected soils across different treatments.

1. Introduction

Exploiting saline-alkali land is increasingly considered to be an important guarantee of global food security. In China, more than 107 hectares of saline-alkali land resources, which include approximately 106 hectares of coastal mudflats, possess favorable governance conditions and high utilization potential in agriculture [1]. Therefore, coastal mudflat salt-affected soils are viewed as an important reserve resource of arable land, and have been amended in recent years to alleviate the problem of the growing scarcity of cultivated land [2,3]. However, newly reclaimed coastal mudflat salt-affected soil is characterized by underdeveloped soil with poor structure, high salinity, low content of soil organic carbon (SOC), and a saline-alkali stressed and nutrient-constrained soil microbiome [4,5,6]. Consequently, overcoming the environmental constraints mentioned above is not only crucial to realizing the quality improvement and sustainable development of coastal mudflat soils, but also an important agricultural practice of great significance to guarantee food security.
Among these obstructive factors, the soil microbiome is widely recognized to be an essential factor involved in soil remediation, as the compositional, structural, and functional diversities of soil microbial community are pivotal for soil productivity and sustainability, especially in coastal mudflat salt-affected soils [7,8]. Soil microbiome reassembly is greatly influenced by surrounding environmental factors, such as pH, salinity, and nutrients (i.e., carbon, nitrogen, and phosphorus) [9,10,11]. For example, soil microbial biomass, metabolic activity, population, and community diversity negatively responded to increased soil salinity gradients, while nutritional availability exhibited adverse impacts [12,13,14,15]. Most of the research findings mentioned above were reported in farmlands, and knowledge with respect to the response of the microbial community to environmental changes remains rudimentary in highly salinized coastal mudflat soils, which are generally believed to be distinct from farmlands in soil background microbial flora [15,16,17]. Hence, decoding variations in microbial communities and the underlying mechanisms is beneficial in directionally regulating coastal mudflat ecosystems.
Recently, multitudinous efforts, including physical, chemical, and biological agricultural practices, have been devoted to amending coastal mudflat salt-affected soils. Particularly, fertilizer regimes for SOC improvement purposes, such as exogenous organic ameliorant applications, play an increasingly pivotal role in the shift of soil microbial community in coastal mudflat areas [18,19,20]. On the one hand, SOC plays a crucial role in the formation and stabilization of soil water-stable aggregates, which can effectively block the capillary rise of upward-moving salt and eventually alleviate saline-alkali stress on soil microorganisms [21,22]. On the other hand, SOC can directly affect the growth, metabolic activity, and proliferation of soil microbial populations as the dominant carbon and energy sources, and act as an important determinant of soil microbial community evolution [15,17,23,24]. However, contrasting findings with respect to the influences of organic inputs on soil microbial community were observed due to the various attributes of soil (i.e., soil types and reclamation time) and organic ameliorants (i.e., application types, amounts, and availabilities). For instance, Zhang et al. [25] showed that four-year poultry manure compost application (45,000 kg ha−1 year−1) improved microbial abundance and diversity in salt-affected soil, while Lu et al. [26] reported that the application of rotten straw (12,000 ha−1 year−1) combined with biological fertilizer (1500 kg ha−1 year−1) ameliorated environmental constraints, but reduced the compositional diversity of microbial communities in coastal salt-affected soil. Additionally, Li et al. [17], and Kang et al. [27] found that the effects of sewage sludge (0, 30, 75, and 150 t ha−1) and vermicompost (0, 50, 125, and 250 t ha−1) on the soil microbial community’s compositional, structural, and predicted functional diversities depended on application amounts. Therefore, it is of great significance to comprehensively understand the relationships between organic ameliorants and soil microbial community alterations in coastal mudflats. In the current study, different types of organic ameliorants (sewage sludge and sludge-based vermicompost) at different application amounts (0, 50, 100, and 200 t ha−1) were selected according to previous studies [15,28,29] to disentangle how ameliorant-amended environmental factors operate in bacterial community reassembly in coastal mudflat salt-affected soils.

2. Materials and Methods

2.1. Experimental Site, Sewage Sludge, and Sludge-Based Vermicompost

The field trial of this study was performed in Tiaozini, Dongtai city, Jiangsu province, China (E 120°56′51″, N 32°49′56″). This region has a northern subtropical continental monsoon climate. The mean annual temperature is 14.6 °C, and mean annual rainfall is 1417 mm. The soil of the experimental site is representative salt-affected soil, and the basic chemical characteristics are shown in Table S1.
The sewage sludge and sludge-based vermicompost used in the present study were purchased from the Jiangsu Chunguang earthworm cultivation company. They were adequate for land application because the main chemical parameters of sewage sludge and sludge-based vermicompost met the criteria specified in the Chinese National Standards (CNS, GB/T 24600–2009). The basic chemical characteristics of sewage sludge, sludge-based vermicompost, and relevant CNS are shown in Table S1.

2.2. Experimental Design and Soil Sampling

Seven treatments belonging to three groups were used in this study. The first group: (1) CK, coastal mudflat salt-affected soil amended without organic ameliorants; the second group included three treatments: (2–4) salt-affected soil amended by sewage sludge at the application rates of 50 (S50), 100 (S100), and 200 t ha−1 (S200); the third group included three treatments: (5–7) salt-affected soil amended by vermicompost at the application rates of 50 (V50), 100 (V100), and 200 t ha−1 (V200). The application amounts of sewage sludge and vermicompost were determined by comprehensively considering the average contents of organic matter in cropland soil (0.5–1.5%), coastal salt-affected soil, sewage sludge, and the vermicompost used in the current study. Each treatment comprised three randomly distributed experimental plots, and each plot was 4 m long and 4 m wide. Organic ameliorants were one-time basal applicated into the test plots and evenly mixed with topsoil (0~20 cm) using a walking rotary cultivator in October 2019. The soils of all treatments were sampled from each microplot at the depth of 0–20 cm [19,30] in October 2020.
The collected soils were immediately taken back to the laboratory and divided into three subsamples after visible plant and organic debris, stones, and litter had been carefully removed using forceps. One batch of soil was stored at 4 °C for the following soil enzyme activity measurement; one batch of soil was sieved (2 mm sifter) and air-dried for further chemical properties determination; the remaining soil was sieved (2 mm sifter) and stored at −80 °C for subsequent microbial analysis.

2.3. Soil Physicochemical and Enzymatic Assays

Soil chemical characteristics, including pH, salinity, SOC, total nitrogen (TN), total phosphorus (TP), available N (AN), and available P (AP), were determined in this study according to the methods described by Li et al. [17]. Total microbial activity was characterized with the method of fluorescein diacetate (FDA) hydrolysis and expressed as the fluorescein production (μg) produced by the reaction of microbial metabolites with fluorescein sodium salt per gram of dry soil per hour [31]. In addition, enzyme activities closely related to soil carbon (sucrase, SUC), nitrogen (urease, URE), and phosphorus (phosphatase, ALP) cycling processes were determined using 3,5-dinitrosalicylic acid colorimetry, the sodium phenol-sodium hypochlorite colorimetric method, and the phenyl phosphate colorimetric method, respectively. In the current study, SUC, URE, and ALP activities are expressed as the contents of glucose, NH3-N, and phenolic substances in 1 g of dry soil after incubation for 24 h, respectively.

2.4. DNA Extraction, Real-Time Quantitative PCR, and 16S rDNA Amplicon Sequencing

For each soil sample, microbial DNA was separately isolated from 500 mg of fresh soil using FastDNA® SPIN Kit (MP Biomedicals, Santa Ana, CA, USA) following the manufacturer’s protocols. Then, the isolated DNA extractions were stored at −80 °C after quantity and purity determinations [15].
Bacterial abundance was quantified on a MiniOpticon™ Real-Time PCR System (Bio-Rad Laboratories Inc., Hercules, CA, USA). The 20 μL mixture contained 1 μL DNA template, 10 μL SYBR Green qPCR Master Mix (2×), 0.4 μL forward primer (341-F, 5′-CCT ACG GGA GGC AGC AG-3), 0.4 μL reverse primer (518-R, 5′-ATT ACC GCG GCT GCT GG-3′), and 8.2 μL ddH2O. The amplification procedures of real-time PCR were as follows: initial denaturation at 95 °C for 2 min, followed by 39 cycles of denaturation at 98 °C for 30 s, annealing at 58 °C for 30 s, extension at 72 °C for 30 s, and a final extension at 72 °C for 5 min [32].
Illumina Miseq sequencing was applied to characterize the compositional and structural diversities of bacterial communities across the different soil samples. In this study, the V4 region of bacterial 16S rDNA was amplified using primer pairs 515-F (5′-GTG CCA GCM GCC GCG GTA A-3′) and 806-R (5′-GGA CTA CHV GGG TWT CTA AT-3′) with the PCR reaction details described by Zhao et al. [33]. PCR products were pooled into equimolar and then purified using AMpure XP beads. Paired-end sequencing was performed on an Illumina Miseq instrument at Genesky Biotechnology Co., Ltd., Shanghai, China. Raw sequences obtained from Illumina Miseq sequencing were quality-controlled, merged, and analyzed according to the established procedures of Li et al. [31]. Lastly, the filtered sequences were rarefied at a unified depth (70,000) across different treatments for subsequent community diversity analysis.

2.5. Bioinformatics Analysis and Statistical Analysis

The compositional (Shannon) diversity of bacterial communities was calculated to characterize the differences in bacterial communities among different treatments using QIIME (version 1.9.1, Maryland, DC, USA). To compare the dissimilarity of structural diversity across all treatments, principal coordinates analysis (PCoA) and hierarchical cluster analysis were performed on the basis of Bray–Curtis distance matrices. For bacterial community compositions, heatmaps were used to visualize the dominant bacterial phyla and families with higher average relative abundances across all treatments using the Pheatmap R package. Furthermore, Statistical Analysis between Metagenomic Profiles (STAMP, version 2.1.3) was used to detect significantly enriched or reduced bacterial phyla between each organic ameliorant-treated soil and control soil (two-sided Welch’s t-test with 95% confidence intervals). In this study, OTUs that presented in any one replicate of each treatment were defined as core OTUs, and OTUs that appeared only in one treatment were defined as unique OTUs. Co-occurrence networks in the control, and sewage sludge- and vermicompost-amended soils were constructed and visualized (Gephi, version 0.9.2) to reveal the correlations between strongly (r > 0.6, p < 0.05) correlated core OTUs using the igraph and Hmisc packages. Redundancy analysis (RDA) and Monte Carlo permutation tests (n = 999) were conducted to reveal the environmental factors driving the dissimilarities in soil bacterial communities across different treatments. Significant differences in soil physicochemical properties, bacterial abundances (log10-transformed), enzyme activities, Shannon diversities, and bacterial community taxonomic compositions were tested using one-way ANOVA, followed by Duncan’s test at the 5% level. The effects of organic ameliorants types (sewage sludge and sludge-based vermicompost) and application amounts (50, 100, and 200 t ha−1) on soil abiotic and biotic characteristics were evaluated using multiple analyses of variance (MANOVA).

3. Results

3.1. Compositional and Structural Diversities of Bacterial Communities

Quantitative PCR results show that the bacterial populations in sewage sludge and sludge-based vermicompost treatments were significantly (p < 0.05) higher than that in CK (Figure 1A), with the highest abundance observed in the S200 treatment. Organic ameliorants exhibited significant (p < 0.05) influence on the compositional diversity of bacterial communities in coastal mudflat salt-affected soil (Figure 1B and Table S2). In particular, the Shannon diversities of bacterial communities in most organic ameliorant-amended soils declined with significantly lower measurements observed in the S100, S200, V50, and V100 treatments as compared to that in CK.
PCoA shows that sewage sludge and sludge-based vermicompost significantly (p < 0.05) altered the bacterial structural diversities of coastal salt-affected soil (Figure 1C and Table S2). In general, both sewage-sludge- and sludge-based vermicompost-amended soils harbored distinctive bacterial community structures as compared to untreated soil. Furthermore, different application amounts of the two organic amendments exhibited obvious dose effects on soil bacterial community distributions in the biplot. Hierarchical cluster analysis further reveals that coastal mudflat soils amended by higher amounts of sewage sludge (S100 and S200) and vermicompost (V100 and V200) clustered together, respectively, and significantly separated from CK treatment (Figure 1D).

3.2. Taxonomic Compositions of Soil Bacterial Community

Organic ameliorants significantly (p < 0.05) modulated the bacterial community from the family to the phylum level (Figures S1 and S2). Particularly, Proteobacteria, followed by Chloroflexi, Bacteroidetes, and Acidobacteria, were the dominant phyla across all the treatments (Figure S1A). Families Xanthomonadaceae, Pelobacteraceae, Sinobacteraceae, and Cytophagaceae were the dominant families across all the treatments (Figure S1B). STAMP shows that Actinobacteria and Proteobacteria were significantly enriched in sludge- and vermicompost-amended soils, while relative abundances of Chloroflexi were significantly depleted as compared to CK (Figure S2).
Organic ameliorants significantly (p < 0.05) drove the reassembly of soil core and unique bacterial microbiomes (Table 1 and Figure 2). Core OTUs in all treatments were 193, and accounted for 2.2–4.3% of the retained OTUs, and 7.5–17.2% of the retained sequences (Table 1 and Table S3). Core OTUs were affiliated into 36 families across different treatments. Specifically, Pelobacteraceae was the dominant family with the highest average relative abundances across all treatments. Families Cytophagaceae, Pseudomonadaceae and Nitrososphaeraceae in S-amended soils, and Ignavibacteriaceae in V-amended soils were enriched as compared to CK (Figure 2A).
Organic ameliorants considerably altered unique bacterial microbiomes as compared to the CK treatment. The total number of unique OTUs in all treatments was 21,459, accounting for 42.8–64.9% of the retained OTUs, and 24.3–51.7% of the retained sequences (Table 1 and Table S3). Unique OTUs in different treatments were subordinate to 52 families. Particularly, the most abundant unique families in different treatments were Pirellulaceae (CK, S50, and V200), Xanthomonadaceae (S100, S200), and Hyphomicrobiaceae (V50). Specifically, OTUs belonging to Microthrixaceae, Actinosynnemataceae, and Eubacteriaceae were only found in sewage sludge-amended soils, while species classified into the Methylocystaceae, Mycobacteriaceae, and Pseudonocardiaceae families were only observed in vermicompost-amended soils (Figure 2B).

3.3. Co-Occurrence Networks of Core Microbiomes

Results show that soils after different organic ameliorant amendments harbored considerably distinct co-occurrence networks of bacterial core microbiomes (CK vs. S vs. V) (Figure 3 and Table 2). Specifically, organic ameliorants significantly altered soil bacterial keystone taxa (core OTUs with top 10 degrees), with distinct keystone OTUs observed in S- and V-amended coastal salt-affected soils as compared to the CK treatment (Figure 3). For instance, bacterial keystone OTUs belonging to Bacillus (OTU3), Microbulbifer (OTU4), and Steroidobaouter (OTU17) were found in untreated coastal salt-affected soil, while bacterial groups comprised Bacillales (OTU13), Bacillus (OTU3), and Flavobacterium (OTU34), and bacterial guilds contained Alphaproteobacteria (OTU55), Nitrospiraceae (OTU94), and Ignavibacteriaceae (OTU49) enriched in sewage-sludge- and vermicompost-treated soils, respectively. Additionally, there were 113, 84, and 153 nodes in the control, and sewage-sludge- and vermicompost-amended soils, respectively. Compared with CK, more edges, and a greater average degree and network diameter were observed in organic ameliorant-amended soils, especially the vermicompost treatment. Interestingly, a lower modularity and average clustering coefficient were found in organic ameliorant treatments as compared to the CK treatment (Table 2).

3.4. Driving Factors of Bacterial Community Differentiation in Coastal Mudflat Salt-Affected Soil

Overall, lower soil pH and salinity, and higher contents of nutrients (C, N, and P) and enzyme activities were observed in organic ameliorant treatments as compared to the CK treatment (Tables S4 and S6). Additionally, the application types, amounts, and their interactions of organic ameliorants exhibited significant (p < 0.05) effects on most soil physicochemical properties and soil enzyme activities (Tables S5 and S7). In the current study, RDA was conducted to reveal the determinant factors among physicochemical and enzymatic attributes in driving bacterial community differentiation in coastal salt-affected soil (Figure 4). Results show that the abiotic and biotic factors mentioned above explained 78.05% of the total bacterial community variation in soils under different treatments. Among these factors, soil pH, salinity, SOC and TP, and the activities of SUC, URE, and ALP were the predominant determinants with respect to the reassembly of the bacterial communities in soils after different organic ameliorants amendments.

4. Discussion

Increasing evidence demonstrates that organic input managements can significantly alter soil biological properties, especially soil microbial communities [34,35]. In the current study, significantly higher bacterial abundances, observed in organic amendment-treated soils as compared to CK treatment (Figure 1A), were in accordance with previous studies in which both sewage sludge [36] and vermicompost [37] significantly improved soil bacterial populations in different soil types. When taking the nutrition deficiency in coastal salt-affected soil into account, the reason lies in the fact that the application of sewage sludge and sludge-based vermicompost with abundant nutrient sources (i.e., carbon, nitrogen, and phosphorus) offered favorable conditions for microbial proliferation. Interestingly, significantly lower Shannon diversities of bacterial communities were observed in all organic ameliorant-treated soils (Figure 1B), which was similar to the observations of Jiang et al. [5], who also found that the bacterial compositional diversity in coastal salt-affected soil negatively responded to organic input management. This may have partially been due to the selective promotion or inhibition on specific microorganisms mediated by relatively specific carbon sources contained in different types of organic amendments [10,38]. For instance, significantly enriched Proteobacteria were detected in most of the organic ameliorant-amended soils as compared to CK (Figures S1 and S2), suggesting that ameliorative soil nutritional conditions are conducive to the flourishment of Proteobacteria, as they are widely reported to be eutrophic microorganisms [39,40]. On the other hand, significantly depleted Chloroflexi, Acidobacteria, and Planctomycetes were observed in these amended coastal salt-affected soils, which was likely because the relative abundances of these oligotrophic microorganisms are negatively correlated with soil nutrient content [41,42,43,44]. Besides the compositional diversity, distinct bacterial community structures, and distinguishable core and unique microbiomes were observed in the sewage-sludge- and sludge-based vermicompost-amended soils as compared to CK (Figure 1C,D and Table 1). This is consistent with the previous findings of Jiang et al. [5], and Li et al. [17], who also found that both types and application rates of organic amendments are important influencing factors in the reassembly of soil bacterial microbiome.
Co-occurrence networks can reveal the interactions of microorganisms among soil microbial communities and are increasingly viewed as a robust indicator for estimating the influences of reassembled soil microbiomes on multiple soil functions under different environmental constraints [45,46,47]. In our study, distinct profiles of networks with differentiated keystone OTUs affiliated to different bacterial taxa were found across different treatments (Figure 3 and Table 2), which indicates that both sewage sludge and sludge-based vermicompost significantly altered the interactions of bacterial core microbiomes in coastal mudflat soil, and strongly implies that the functional capabilities of mudflat soil might have been changed as a result of the application of the two organic amendments. Specifically, bacterial groups with closer linkages and versatile functional potentials were enriched in organic ameliorant-amended soils, such as Bacillus, Flavobacterium, and Rhodothermaceae in sewage sludge treatments, and Alphaproteobacteria, Pseudomonas, Nitrospiraceae, and Ignavibacteriaceae in sludge-based vermicompost-treated soils (Figure 3). These findings imply that sewage sludge and sludge-based vermicompost are conducive to the reassembly of bacterial core microbiomes with improved and various functionalities in coastal mudflat soils, as these bacterial taxa are widely reported to play crucial roles in soil function maintenance and quality improvement [48,49,50,51,52]. Additionally, more nodes with closer interactions (edges) but lower modularity, which were observed in organic amendment-treated soils (Table 2), indicate the formation of bacterial guilds with a larger scale but less stability in the two soils as compared to the nontreated coastal salt-affected soils [53,54]. These results are further supported by the larger diameter but lower average clustering coefficient of networks in the two amended soils (Table 2). These findings are similar to the previous findings of Zhao et al. [55], who also found bacterial communities to have lower stability and distinct interactions among community members in response to a sewage sludge amendment, as also described by de Vries et al. [56]. Sludge-based vermicompost exhibited more pronounced effects on soil bacterial interactions as compared to sewage sludge (Table 2). Considering the profound impact of earthworm activity on the physicochemical properties of sewage sludge, these results were likely because more available patterns and contents of carbon and energy sources were introduced by sewage sludge into coastal salt-affected soil, and favored the growth and reproduction of soil microorganisms [57,58].
The application of organic amendments is increasingly confirmed to be able to efficiently alleviate obstacle factors of the development and sustainable utilization of coastal mudflat areas [59,60,61]. Both sewage and vermicompost significantly improved the soil quality of coastal mudflats with ameliorated salt and alkaline stresses, and enhanced nutrient availability and enzyme activity (Tables S4 and S6), which is similar to the previous reports of Bai et al. [21], and Arancon et al. [62], who also suggested that the application of the two organic amendments might be a viable and efficient agricultural practice for the amelioration of coastal salt-affected soils. The impact of sewage sludge and vermicompost had evident dosage effects on coastal mudflat soil’s pH, salinity, nutritional contents, and enzyme activities (Tables S5 and S7). Consistent with previous studies, more organic acids derived from organic matter decomposition and more nutrients introduced by higher application amounts of organic amendments might be responsible for the dose effect induced by organic inputs on salt-affected soil amelioration [17,63,64]. Additionally, the regulative and progressive effect of sewage sludge on the physicochemical characteristics of mudflat soil is more pronounced than that of sludge-based vermicompost, which might be explained by the differentiations of physicochemical characteristics between sewage sludge and sludge-based vermicompost (Table S1) [65].
Numerous studies demonstrated that the compositional and structural diversity of microbial communities is greatly influenced by variations in their microhabitats harboring different environmental attributes, especially saline-sodic soils [66,67]. Unsurprisingly, RDA results reveal that the environmental factors determined in current study drove the reassembly of bacterial microbiomes in coastal salt-affected soils under different treatments (Figure 4). Among these factors, SOC significantly affects the formation of bacterial microbiomes in soils under different treatments. Abundant and diverse carbon sources might directly motivate the differentiation of bacterial communities in different soils. Apart from the direct effects, SOC is also capable of indirectly facilitating the reassembly of soil bacterial microbiomes due to its positive effects on the amendment of soil environmental constraints (e.g., poor soil structure and saline-alkali stress) [15,17]. Additionally, enzyme activities (i.e., SUC, URE, and ALP) that are linked to carbon, nitrogen, and phosphorus cycling processes exhibited significant influence on bacterial microbiome variation in different soils. The reason was likely due to the fact that these extracellular enzymes contributed to the enhancement of nutrient availability and the flourishment of microorganisms possessing relevant catabolic activities, which eventually drove the shift of the soil microbial communities under different treatments [68,69]. Soil pH and salinity were also significant driving determinants and showed the opposite effects on soil bacterial microbiome assembly as compared to those of SOC and enzyme activities (Figure 4). These results are likely attributed to the soil microbial community positively responding to the decline in pH and salinity induced by the application of organic ameliorants, as most microorganisms are pH- and salinity-intolerant in coastal salt-affected soil with severe saline-alkali stress [70,71,72].

5. Conclusions

In conclusion, this study provides evidence that organic ameliorants (sewage sludge and sludge-based vermicompost) can mitigate saline-alkali stress, nutrient deficiency, and limited enzyme activity, and thereby enable bacterial microbiome reassembly in coastal mudflat salt-affected soil. Moreover, application types and amounts, and their interactions with organic ameliorants exhibited significant influences on abiotic and biotic attributes of coastal mudflat salt-affected soil. Particularly, the two organic amendments significantly improved bacterial abundance, but reduced bacterial compositional diversity. Sewage sludge- and vermicompost-amended soils harbored distinct core and unique bacterial microbiomes as compared to untreated coastal salt-affected soil. Specifically, vermicompost exhibited more pronounced effects on the scale expansion, interaction enhancement, and stability reduction of core bacterial guilds as compared to sewage sludge. Additionally, the positive effects of organic inputs on the alleviation of environmental constraints were enhanced with the increase in the amount of organic ameliorant application. RDA indicates that soil abiotic (e.g., pH, salinity, and SOC.) and biotic (e.g., sucrase, urease, and phosphatase) factors are significant determinants driving the alterations in the bacterial communities’ compositional and structural diversity. These outcomes contribute to enhancing the relevant knowledge about organic ameliorant-related coastal salt-affected soil reclamation from physicochemical and microbial aspects.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12102525/s1. Table S1: main physicochemical properties of mudflat soil, sewage sludge, and sludge-based vermicompost used in the present study; Table S2: effects of application types and amounts of organic ameliorants on compositional and structural diversities of soil bacterial community; Table S3: percentages of unique and core OTUs, and their corresponding sequences; Table S4: physicochemical properties of soil samples under different treatments; Table S5: effects of the application types and amounts of organic ameliorants on soil physicochemical characteristics; Table S6: effects of sludge and sludge vermicompost on soil enzyme activities; Table S7: effects of material and additive amount on soil enzyme activities. Figure S1: bacterial community compositions among different treatments; Figure S2: STAMP of significantly enriched and declined bacterial phyla in each organic ameliorant-amended soil as compared to untreated coastal mudflat salt-affected soil.

Author Contributions

Y.L.: data analysis, visualization, writing—original draft preparation. Y.W.: experiments, data curation, and software. C.G. and Z.Z.: manuscript revision. C.S., L.X., Y.Z. and S.Y.: methodology and formal analysis. W.Z.: supervision. Y.S. and Y.B.: conceptualization and funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (41977089), Key Laboratory of Organic Geochemistry, GIGCAS (SKLOG202118), Fund for the State Key Laboratory of Pollution Control and Resource Utilization (PCRRF21036), the Research Fund for Jiangsu Agricultural Industry Technology System (JATS[2022]352, JATS[2022]353, and JATS[2022]354) for Yanchao Bai, the National Natural Science Foundation of China (31872179) for Yuhua Shan, and the Blue-Blue Project and High-Rank Talent of Yangzhou University and Jiangsu Province.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The analyzed datasets in the present study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Effects of organic ameliorants on compositional and structural diversities of soil bacterial community. (A) Soil bacterial abundance; (B) Shannon diversity of bacterial community; (C,D) PCoA and hierarchical cluster analysis of bacterial communities in different soils, respectively. Different letters on bars represent significantly different at p < 0.05 according to Duncan’s multiple-range test.
Figure 1. Effects of organic ameliorants on compositional and structural diversities of soil bacterial community. (A) Soil bacterial abundance; (B) Shannon diversity of bacterial community; (C,D) PCoA and hierarchical cluster analysis of bacterial communities in different soils, respectively. Different letters on bars represent significantly different at p < 0.05 according to Duncan’s multiple-range test.
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Figure 2. Relative abundances of (A) bacterial core and (B) unique OTUs in soils under different treatments. Top 20 core and unique bacterial families are presented. Asterisks (*) indicate significant differences among treatments according to Duncan’s multiple-range test (p < 0.05).
Figure 2. Relative abundances of (A) bacterial core and (B) unique OTUs in soils under different treatments. Top 20 core and unique bacterial families are presented. Asterisks (*) indicate significant differences among treatments according to Duncan’s multiple-range test (p < 0.05).
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Figure 3. Co-occurrence networks of bacterial core microbiomes in soils under different treatments. Control group (CK); sludge treatment (S); vermicompost treatment (V). Keystone taxa, defined by the core OTUs with top 10 degrees, are labeled in black.
Figure 3. Co-occurrence networks of bacterial core microbiomes in soils under different treatments. Control group (CK); sludge treatment (S); vermicompost treatment (V). Keystone taxa, defined by the core OTUs with top 10 degrees, are labeled in black.
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Figure 4. Redundancy analysis (RDA) of soil physicochemical properties and enzyme activities on bacterial community structure. “*” and “**” indicate p < 0.05 and p < 0.01, respectively.
Figure 4. Redundancy analysis (RDA) of soil physicochemical properties and enzyme activities on bacterial community structure. “*” and “**” indicate p < 0.05 and p < 0.01, respectively.
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Table
Table 1. The number of core and unique OTUs in different treatments.
Table 1. The number of core and unique OTUs in different treatments.
TreatmentsCKS50S100S200V50V100V200
CK3815
S5019232906
S100137713232803
S2001081118616033144
V50148911048987613047
V10088461549543710572904
V20022541501104478211827042840
Core OTUs193193193193193193193
Total OTUs8916585055045555557144795783
Table
Table 2. Topological properties of bacterial co-occurrence network.
Table 2. Topological properties of bacterial co-occurrence network.
Topological CharacteristicsCKSV
Number of nodes11384153
Number of edges1101421118
Average degree1.9473.38114.614
Network diameter1108
Modularity0.9520.6430.257
Average clustering coefficient10.4270.586
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Li, Y.; Wang, Y.; Gu, C.; Shen, C.; Xu, L.; Zhao, Y.; Yi, S.; Zuo, W.; Shan, Y.; Zhang, Z.; et al. Differential Effects of Organic Ameliorants on the Reassembly of Bacterial Communities in Newly Amended Coastal Mudflat Salt-Affected Soil. Agronomy 2022, 12, 2525. https://doi.org/10.3390/agronomy12102525

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Li Y, Wang Y, Gu C, Shen C, Xu L, Zhao Y, Yi S, Zuo W, Shan Y, Zhang Z, et al. Differential Effects of Organic Ameliorants on the Reassembly of Bacterial Communities in Newly Amended Coastal Mudflat Salt-Affected Soil. Agronomy. 2022; 12(10):2525. https://doi.org/10.3390/agronomy12102525

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Li, Yunlong, Yimin Wang, Chuanhui Gu, Chao Shen, Lu Xu, Yilin Zhao, Siqiang Yi, Wengang Zuo, Yuhua Shan, Zhuqing Zhang, and et al. 2022. "Differential Effects of Organic Ameliorants on the Reassembly of Bacterial Communities in Newly Amended Coastal Mudflat Salt-Affected Soil" Agronomy 12, no. 10: 2525. https://doi.org/10.3390/agronomy12102525

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