Spatiotemporal Variations in Soil Organic Carbon and Microbial Drivers in the Yellow River Delta Wetland, China

Abstract

This study explores the spatiotemporal dynamics of SOC and microbial-mediated mechanisms in the Yellow River Delta wetlands. Using redundancy analysis and microbial community profiling, we show that vegetation drives distinct SOC storage patterns: Phragmites australis ecosystems exhibit the highest SOC sequestration, followed by Suaeda salsa and Tamarix chinensis habitats, where salt-tolerant taxa like Desulfobacterota and Halobacteriaota promote short-term carbon storage via anaerobic metabolism. The microbial community structure is shaped by both vegetation-induced microhabitats and environmental gradients: SOC and total nitrogen dominate community assembly, while electrical conductivity, pH, and sulfur/nitrogen nutrients regulate spatiotemporal differentiation. Seasonal turnover drives the reorganization of microbial community structures, shaping the dynamic equilibrium of carbon pools. Seasonal DOC dynamics, linked to tidal fluctuations and exogenous carbon inputs, highlight hydrology’s role in modulating active carbon pools. These findings reveal tight linkages among vegetation, microbial functional guilds, and soil biogeochemistry, critical for wetland carbon sequestration.

1. Introduction

As one of the most highly productive ecosystems on Earth, wetlands play a critical role in the global carbon cycle as substantial carbon sinks [1]. Often referred to as the “kidneys of the Earth”, wetlands are among the most biologically productive and ecologically valuable ecosystems on the planet. Covering approximately 6% of Earth’s terrestrial surface, they play a disproportionate role in global biogeochemical cycles, particularly the carbon cycle [2]. These ecosystems store an estimated 20–30% of the world’s soil organic carbon (SOC) despite their limited spatial extent, making them critical for mitigating climate change through long-term carbon sequestration [3,4]. However, the stability and distribution of SOC in wetlands are highly dynamic, shaped by a complex interplay of biotic and abiotic factors [5,6]. Among these, vegetation types and microbial communities are increasingly recognized as pivotal drivers of SOC dynamics, yet their synergistic interactions and site-specific mechanisms remain poorly understood, especially in deltaic wetlands experiencing rapid environmental changes [7]. The Yellow River Delta (YRD) in China, a UNESCO-protected wetland of international importance, exemplifies such a dynamic system. Formed by the interplay of fluvial sedimentation, tidal forces, and anthropogenic interventions, this supports a mosaic of plant communities, ranging from salt-tolerant Suaeda salsa to Phragmites-dominated Phragmites australis marshes and Tamarix chinensis shrublands, each creating distinct microhabitats with unique biogeochemical properties.

Wetlands absorb carbon through two primary pathways: long-term carbon sequestration from the accumulation of organic matter in plant biomass (roots, litter, and exudates) and short-term carbon storage due to anaerobic soil conditions that inhibit microbial decomposition [8]. In autumn, plant growth slows down, the input of plant detritus increases, and microbial communities shift from a “growth type” to a “storage type”. This process may gradually convert the peak autumn biomass carbon into long-term carbon sequestration. Globally, peatlands and coastal wetlands are particularly efficient at long-term carbon sequestration, with some systems preserving organic matter for millennia [9,10]. However, deltaic wetlands like the YRD present a paradox: their high productivity and rapid sedimentation rates suggest strong carbon sequestration potential, yet their dynamic hydrology and salinity gradients create heterogeneous environments where carbon stabilization mechanisms are less predictable [11]. The YRD’s unique geomorphology, characterized by frequent channel shifts, sediment redistribution, and tidal inundation, creates a patchwork of soil conditions [12]. For instance, Phragmites australis areas typically occupy lower-lying, frequently flooded areas with fine-textured soils, whereas Suaeda salsa thrives in higher-elevation, saline–alkaline soils [13]. These vegetation patterns directly influence SOC distribution by modulating organic matter inputs and soil redox conditions [14]. However, recent studies highlight that microbial communities, which mediate SOC decomposition and stabilization, are equally critical in determining whether carbon is retained as stable organic matter or lost as CO₂ or CH₄ [15].

In the YRD, plant communities are the dominant forces shaping landscapes and ecological processes. Different plant species exhibit various functional traits, such as growth rate, root morphology, and litter quality, all of which directly or indirectly influence organic carbon dynamics [16,17]. For example, plants with extensive root systems enhance soil aggregation and create microenvironments conducive to carbon stability, while other species contribute varying quantities and qualities of litter input, affecting the rate of organic matter decomposition [18,19]. Additionally, microbial communities, as key drivers of soil biogeochemical processes, are closely linked to the transformation of SOC [20,21]. Microorganisms decompose organic matter, release nutrients, and either promote or hinder carbon sequestration depending on their metabolic activities [22]. The composition and diversity of wetland microbial communities are regulated by plant root exudates, soil physicochemical properties, and other environmental factors [23,24]. However, the YRD faces unprecedented pressures from climate change (e.g., sea level rise, increased salinity intrusion) and human activities (e.g., oil extraction, land reclamation), which threaten its carbon sequestration capacity [25,26].

In the context of global warming, changes in rainfall distribution, leading to drought or seasonal waterlogging, will alter the soil and atmospheric humidity environments, regulate plant physiological and metabolic processes, and ultimately affect the blue carbon function of coastal wetlands [27]. At the same time, sea level rise leads to an increased frequency and intensity of tidal incursions, submerging low-lying wetlands, disrupting plant root environments, and accelerating soil erosion and salinization. Wetland degradation results in decreased vegetation cover, reducing the input of SOC, while enhancing the microbial decomposition rates of organic carbon, leading to increased carbon release. Furthermore, increased salinity inhibits the growth of freshwater plants and promotes the expansion of salt-tolerant plants, and these changes in vegetation types lead to alterations in the quality of carbon inputs to the soil [28]. At the same time, salinity stress affects the microbial community structure, inhibiting decomposer activity or promoting the growth of halophilic bacteria, potentially delaying or accelerating carbon decomposition [29,30].

In recent years, the YRD Nature Reserve has faced severe challenges in wetland degradation and carbon sink protection yet has significantly improved SOC dynamics through ecological restoration efforts. The degradation of the YRD wetlands is primarily caused by the invasion of Spartina alterniflora, land reclamation, and ground subsidence. The invasion of Spartina alterniflora has resulted in the severe degradation of native vegetation and a decline in biodiversity. However, in recent years, through the management of Spartina alterniflora, the conversion of cropland to wetlands, and vegetation restoration, the wetland protection rate in the YRD has increased to 60.47%, with significant recovery in vegetation coverage. Therefore, understanding how plant–microbe interactions regulate the distribution of organic carbon in this region is not only a scientific necessity but also a practical requirement for sustainable wetland management.

This study hypothesizes that plant types, represented by dominant species such as Phragmites australis, Suaeda salsa, and Tamarix chinensis, together with their associated microbial communities, jointly regulate the accumulation and vertical distribution of SOC. The aim of this research is to reveal the complex relationships among plant traits, microbial community structure, and organic carbon components in the YRD through field sampling and advanced laboratory analysis, thereby providing scientific evidence for sustainable wetland management and climate change mitigation strategies. This will contribute to enhancing the soil carbon sink function of coastal salt marshes and help achieve the goal of carbon neutrality.

2. Materials and Methods

2.1. Study Area

The study area is located in the YRD, Dongying City, Shandong Province, China (118°32′ E–119°20′ E, 37°34′ N–38°12′ N). We selected newly formed sedimentary areas on both sides of the old and new Yellow River mouths (119°07′ E, 37°47′ N) as the research area. The region experiences a continental monsoon climate influenced by the Eurasian continent and the Pacific Ocean, characterized by mild and humid conditions with an average annual temperature of 11.7–12.6 °C and annual precipitation of 530–650 mm. According to data from the China Meteorological Administration, the average annual temperature in the YRD increased by 0.05 °C, and precipitation increased by 13 mm per year from 2000 to 2022, representing the highest growth rate in the Yellow River Basin. Historical data show that from 1961 to 2007, spring precipitation in the YRD exhibited a decreasing trend, leading to a rise in soil salinity above 20‰ and a 37% reduction in reed photosynthetic intensity. Precipitation is primarily concentrated in the summer, often occurring as heavy rainfall. In the summer of 2023, precipitation accounted for over 60% of the annual total, resulting in an increased risk of short-term flooding in wetlands and potentially triggering surface runoff erosion, which could accelerate soil carbon loss. The wetland vegetation in the YRD is highly diverse, encompassing various ecological types and providing a critical habitat for numerous plant and animal species. With a natural vegetation coverage of 55.1%, it constitutes the largest newly formed wetland vegetation zone along China’s coast, playing a pivotal role in carbon sequestration and biodiversity conservation.

2.2. Soil Sampling and Processing

The field investigation was conducted in October 2021 (autumn, vegetation maturation period) and May 2022 (spring, growing period). Considering the influence of hydrological and salinity gradients on vegetation community distribution, samples were collected along a gradient from humid freshwater to arid saline–alkali and finally to coastal hypersaline environments. Three typical vegetation communities were selected in the study area: Phragmites australis community, Tamarix chinensis community, and Suaeda salsa community (Figure 1). Given that the storage of SOC shows the greatest variation in the 0–1 m soil layer, while it stabilizes at depths greater than 1 m, we collected soil samples at two depths, 0–20 cm and 20–60 cm, with five replicate samples taken at each depth. The samples were divided into two portions: one portion of fresh soil was used to analyze the soil moisture content (MC), ammonium nitrogen (NH₄⁺-N), nitrate nitrogen (NO₃⁻-N), and dissolved organic carbon (DOC); the other portion, after air-drying and sieving, was analyzed for soil pH, electrical conductivity (EC), soil organic carbon (SOC), total phosphorus (TP), and total nitrogen (TN).

2.3. Laboratory Analysis

The SOC content was determined using the potassium dichromate oxidation heat treatment method. A specified amount of air-dried, sieved (0.25 mm) soil sample was weighed, and an excess of potassium dichromate–sulfuric acid solution was added. The mixture was heated in an oil bath to oxidize SOC to carbon dioxide. The remaining potassium dichromate was then titrated with a standardized ferrous sulfate solution, and the SOC content was calculated based on ferrous sulfate consumption. DOC was measured by the total organic carbon analyzer (TOC-2000, METASH, Shanghai, China).

Soil pH and EC were determined via the glass electrode method. The MC was measured using the gravimetric method; the TN content was analyzed via the Kjeldahl method. TK was measured with a flame photometer, and TP was quantified using the molybdenum–antimony colorimetric method. Additionally, NO₃⁻-N and NH₄⁺-N were analyzed using ion chromatography to comprehensively assess the effects of soil physicochemical properties on SOC distribution.

2.4. DNA Extraction and Sequence Analyses

The Magnetic Soil and Stool DNA Kit for soil (Qiagen, Valencia, CA, USA) was used to extract DNA from 0.5 g homogenized soil. The bacterial 16S rRNA and fungal ITS genes were amplified using a primer set consisting of 515FmodF and 806RmodR, using polymerase chain reaction (PCR) conditions described by the instructions. PCR products were mixed at equal density ratios, and the mixture was purified using a Qiagen Gel Extraction Kit (Qiagen, Hilden, Germany). The library was constructed with the Illumina TruSeq DNA PCR-Free Library Preparation Kit, quantified by Qubit, and sequenced on the NovaSeq 6000 system. All experimental procedures were conducted by Tianjin Novogen Co., Ltd. (Tianjin, China).

Following sequencing and quality control on the Illumina NovaSeq platform, a total of 358,716 effective tags were obtained from 12 soil samples. The average length of these tags ranged from 418 to 424 bp, accounting for 82.32% of PE reads, with 94.35–95.08% of total bases achieving quality scores ≥ 30. To characterize soil microbial community diversity, composition, and structure, bacterial 16S rRNA genes and fungal ITS regions were amplified. Alpha diversity metrics, including the Simpson and Shannon indices for diversity and Ace/Chao1 estimators for richness, were used to assess microbial community profiles.

2.5. Statistical Analyses

Experimental data were statistically analyzed using SPSS 25.0, with significant differences in wetland soil carbon components across vegetation types tested via the least significant difference (LSD) method at the 0.05 significance level. A diversity matrix was calculated using the QIIME2 core-diversity plugin. Alpha diversity indices (e.g., Shannon, Simpson) at the feature sequence level and β-diversity analyses were performed in QIIME2 to assess sample differences in species composition and complexity. The relationships of soil bacterial communities and the soil environmental variables were determined using redundancy analysis (RDA) in Canoco 5.0.

3. Results

3.1. Soil Characteristics, Carbon Pool, and Carbon Mineralization

Analysis of soil samples between spring and autumn revealed significant seasonal differences in the SOC content, with autumn SOC concentrations exceeding spring levels across all samples (p ≤ 0.05) (Figure 2). Specifically, in Tamarix chinensis and Phragmites australis communities, the autumn SOC content was significantly higher than spring values, whereas no seasonal differences were detected in Suaeda salsa communities. The SOC content across different plant communities followed the order as follows: Phragmites australis > Suaeda salsa > Tamarix chinensis. This divergence may be attributed to the annual lifecycle and shallow rooting depth of Suaeda salsa, which limits its vertical carbon sequestration capacity compared to deep-rooted perennial species like Tamarix chinensis and Phragmites australis, a pattern further supported by the significant correlation between the root biomass and SOC content.

3.2. Variations in Soil Microbial Community Diversity, Composition, and Structure

For the scientific and reliable analysis of microbial community diversity, high-quality sequencing data serve as a critical prerequisite for accurate gene annotation. Microorganisms in spring soil samples were classified into 114 phyla, 215 classes, 408 orders, 524 families, 970 genera, and 459 species, whereas autumn samples comprised 55 phyla, 135 classes, 321 orders, 637 families, 1137 genera, and 486 species. The microbial Alpha diversity in different samples is presented in

Table 1. Microbial Alpha diversity in different samples.

	Sample	ACE	Chao1	Simpson	Shannon	OTU
Spring	LWQ	2219	2209	0.976	8.47	2006
	LWS	4046	4026	0.993	9.42	3635
	JPQ	2507	2502	0.926	8.57	2338
	JPS	3947	4198	0.976	9.06	3617
	CLQ	3776	4410	0.918	8.81	2663
	CLS	2635	3206	0.896	7.12	1450
Autumn	LWQ	4398	4370	0.995	9.82	3687
	LWS	5095	6700	0.996	9.73	3896
	JPQ	3603	3506	0.982	8.18	3027
	JPS	2387	2302	0.962	6.74	2010
	CLQ	4281	4170	0.988	9.05	3732
	CLS	3516	3364	0.964	7.73	2897

.

Analysis of samples from both spring and autumn showed significant spatiotemporal differences in soil microbial communities across the three vegetation communities (LW, CL, and JP). In the Phragmites australis community, both the ACE and Chao1 richness indices significantly increased between seasons. Phragmites australis, with its well-developed root system, facilitates the decomposition of root exudates and litter as rainfall increases during the rainy season, thus providing diverse carbon sources for microorganisms and driving the rise of the ACE/Chao1 indices. The Phragmites australis community maintains high richness and evenness through stable hydrology and multidimensional resources, with seasonal fluctuations primarily driven by hydrology–vegetation coupling [31]. In the Tamarix chinensis and Suaeda salsa communities, the Simpson and Shannon evenness indices indicated a reduction in microbial evenness, primarily due to salt stress selecting for salt-tolerant dominant taxa, which led to dominance by the dominant species. Additionally, the Shannon value in the shallow-soil layer remained consistently higher, possibly due to the anaerobic conditions caused by poor drainage in deeper layers [32].

Seasonal succession re-shapes microbial community assembly by altering temperature–moisture regimes and plant phenological traits, thereby driving changes in rhizodeposition patterns. Within the root microhabitats of distinct vegetation types, microorganisms exhibit spatiotemporally distinct α-diversity patterns through adaptive strategies like metabolic plasticity and differential functional gene expression. This is manifested as vegetation-specific differentiation in richness (ACE, Chao1) and evenness (Shannon, Simpson) indices along soil-depth gradients, highlighting the pivotal role of plant–microbe feedback mechanisms in shaping the spatiotemporal heterogeneity of soil ecosystems.

The relative abundances of soil microbial phyla in spring and autumn are presented in Figure 3. In spring, Proteobacteria and Desulfobacterota exhibited the highest relative abundances across all areas, accounting for 37.83–47.03% and 7.10–9.90% of total soil bacteria, respectively. These values were significantly higher than those of other phyla. Phragmites australis showed greater abundances in both soil depths (0–20 cm and 20–60 cm) of the Phragmites australis community compared to the Tamarix chinensis and Suaeda salsa communities, whereas Desulfobacterota abundances did not differ significantly among the six sampling areas (three vegetation types × two soil depths). The subsequent dominant phyla included Acidobacteriota, Chloroflexi, Gemmatimonadetes, and Bacteroidota.

Intra-seasonal comparisons revealed plot-specific variations in dominant bacterial abundances: only Proteobacteria, Bacteroidota, and Actinobacteriota were more abundant in the Phragmites australis community than in the Tamarix chinensis and Suaeda salsa communities, while all other major phyla exhibited lower abundances in Phragmites. These advantageous microbial communities consist of syntrophic bacteria and plant root-associated symbionts, which participate in the decomposition of plant residues and organic matter. Phragmites australis, by enriching the populations of Proteobacteria, Bacteroidota, and Actinobacteriota, enhances the carbon–nitrogen cycling efficiency of wetlands while inhibiting the acquisition of resources by bacteria from other phyla. The most pronounced difference occurred in Crenarchaeota, a marine archaeal phylum containing Sulfolobales and Desulfurococcales. This phylum accounted for only 0.49–0.77% in the Phragmites australis community, compared to 2.24–2.43% in Tamarix chinensis and 2.68–3.25% in Suaeda salsa. The low abundance of Crenarchaeota in the Phragmites australis community results from a combination of oxygen conditions, resource types, and plant interactions. In contrast, in salt-tolerant plant zones such as Tamarix chinensis, Crenarchaeota may occupy ecological niches through stress tolerance mechanisms, the utilization of recalcitrant carbon, and mixed nutritional strategies.

Phylum-level analysis highlighted two key patterns: (1) distinct compositions of dominant microbial phyla under different vegetation types and (2) within-vegetation variations in phylum abundances across soil layers. These findings underscore the role of vegetation identity and soil depth in shaping the taxonomic structure of microbial communities.

Similarly to in spring, Proteobacteria remained the most abundant phylum in autumn soils, accounting for 21.46–28.66% of total bacteria. The Phragmites australis community exhibited higher abundances than the Tamarix chinensis and Suaeda salsa communities across all soil layers, with no significant vertical differences. Compared to the spring soils, the autumn soils featured additional dominant phyla: Firmicutes, Halobacterota, Campylobacterota, and Cyanobacteria. Among these, Halobacterota, Campylobacterota, and Cyanobacteria showed relatively low abundances, with maximum values across all samples of 5.80%, 3.10%, and 2.60%, respectively. Cyanobacteria and Halobacterota were detected exclusively in the Tamarix chinensis community, while Firmicutes reached their highest abundances in both soil layers of the Tamarix chinensis community (up to 13.93%), significantly exceeding those in the Phragmites australis and Suaeda salsa communities. Desulfobacterota abundance patterns differed between seasons: the maximum value (7.39%) occurred in the shallow soil of the Phragmites australis community in autumn, whereas the overall minimum was observed in the Tamarix chinensis community, opposite to spring trends. At the phylum level, the soil microbial community structure and relative abundances exhibited pronounced temporal differentiation between spring and autumn, reflecting seasonal shifts in dominant taxa and their ecological niches.

In autumn, vegetation reaches maturity, and the phylum Actinobacteria can degrade recalcitrant carbon through the secretion of ligninases, while the phylum Halobacteria maintain cellular osmotic pressure by synthesizing compatible solutes, reflecting the inhibitory effect of high-salinity environments on carbon metabolism. The sulfate concentration in autumn is higher than in spring, providing ample electron acceptors for sulfate-reducing bacteria [33]. The phylum Firmicutes can consume organic matter through dissimilatory sulfate reduction, enhancing the sulfur cycle in the soil. Cyanobacteria fix CO₂ through oxygenic photosynthesis. The seasonal succession of microbial communities is essentially a dynamic coupling of vegetation, environmental factors, and metabolic functions. In autumn, dominant groups regulate the conversion pathways of recalcitrant carbon, striking a balance between short-term carbon release and long-term carbon sequestration [34]. The shift of dominant soil microbial groups from a “vegetation growth-oriented” to a “carbon sequestration-oriented” function is a result of the coevolution of vegetation succession, environmental stress, and microbial metabolism. The restructuring of wetland soil community structure and the optimization of carbon cycling pathways significantly affect the carbon sequestration potential of wetlands.

The heat map of the clusters (Figure 4) obtained after normalization is based on the raw data of soil samples. The horizontal coordinates are the sample names, and each small grid represents a species. The closer the color is to red, the higher the relative abundance of the species; the closer it is to blue, the lower it is. The closer the samples in the clustering tree are to each other, the shorter the branch lengths are, and the more similar the microbial community composition is between the samples.

Figure 4a illustrates that the 15 most abundant bacterial phyla in spring clustered into two distinct branches: the Phragmites australis community (LWQ, LWS) formed an independent cluster, whereas the remaining Suaeda salsa (JPQ, JPS) and Tamarix chinensis (CLQ, CLS) communities constituted the other branch. The distribution of the dominant bacterial phyla exhibited pronounced spatial heterogeneity at the phylum level, with individual dominant phyla also showing intra-layer variation across soil depths. These phyla displayed strong positive abundance correlations in the Phragmites australis community, suggesting functional integration within this vegetation type.

In autumn, cluster analysis grouped CLQ and CLS into one branch, while the remaining four samples formed another branch, indicating high similarity in microbial composition within the group (Figure 4b). This suggests that in autumn, under the influence of waterlogging and salt stress, the roots of tamarisk alleviate shallow-layer salinity by absorbing water from deeper layers, resulting in microbial communities in both the upper and lower soil layers being dominated by slow-decomposing, stress-resistant groups, thereby enhancing functional homogeneity. The dominant phyla are primarily divided into two major ecological groups. The phylum Proteobacteria, closely related to the carbon sequestration process in wetland soils, exhibit the highest abundance correlation in the Phragmites australis community during both seasons. The phylum Proteobacteria are highly correlated with the carbon sequestration process in the Phragmites australis community during both spring and autumn. In spring, they promote vegetation carbon assimilation through root stimulation, while in autumn, they rapidly decompose litter to provide organic matter for long-term carbon sequestration, demonstrating the core role of Proteobacteria in wetland carbon sequestration. In contrast, in the Phragmites australis community, Desulfitobacterium shows peak correlation in autumn, representing seasonal variation that differs from the spring pattern. This phenomenon is attributed to the anaerobic microenvironment formed under waterlogged conditions in autumn, which provides favorable conditions for the growth of Desulfitobacterium. This also demonstrates the Phragmites australis potential for both efficient short-term carbon storage and long-term carbon sequestration. The phylum-level clustering heatmap reveals significant seasonal differences in the composition of dominant microbial phyla and symbiotic networks, highlighting the impact of vegetation types and seasonal dynamics on the microbial community structure.

3.3. Relationships Between the Soil Environment and the Microbial Communities

RDA was conducted to investigate the relationships between spring bacterial communities and soil environmental variables (Figure 5a, detailed data in Supplementary Materials). The first two canonical axes explained 84.5% of the variation in bacterial community composition driven by soil properties. The first RDA axis was strongly correlated with TN and SOC, while the second axis showed a strong association with EC and DOC. Microbial community structure analysis revealed specific correlations: Proteobacteria/Bacteroidota exhibited positive associations with SOC/TN, Desulfobulbia was positively linked to EC, and Acidobacteriota showed negative correlations with both EC and DOC. These results indicate that microbial community composition varies significantly across different environmental gradients, with key soil carbon and nitrogen fractions, alongside salinity (EC), driving bacterial assemblage patterns.

For autumn samples, RDA showed that the first two canonical axes explained 67.2% of the variation in bacterial community composition (Figure 5b, detailed data in Supplementary Materials). The first axis was strongly correlated with TN, SOC, DOC, and TP, while the second axis was more closely associated with EC, pH, and Na⁺. Seasonal divergence in key drivers was evident: Desulfuromonadia exhibited positive correlations with DOC, SOC, and TN, indicating preferential enrichment in high-carbon/nitrogen microhabitats; Gammaproteobacteria and Bacteroidia were positively linked to TN/SOC; and Campylobacteriia and Alphaproteobacteria showed associations with DOC/TP. Comparative analysis revealed significant seasonal differences in the proportion of environmental variation explained, factor–taxon correlation patterns, and interplot community similarity. These findings underscore that the microbial community composition is co-shaped by environmental gradients (e.g., carbon/nitrogen availability, salinity) and vegetation types, resulting in pronounced spatiotemporal heterogeneity in bacterial assemblages [35].

4. Discussion

4.1. Spatiotemporal Distribution Patterns of Wetland SOC Fractions

The dynamics of SOC in the YRD exhibit distinct characteristics compared to in other major deltas worldwide, with carbon sequestration mechanisms and driving factors differing significantly from those in the Mississippi River and Yangtze River deltas. The coastal saline marshes in the YRD have a carbon sequestration capacity of 10 kg/m² per unit area, with an annual carbon sink capacity exceeding 30,000 tons, significantly higher than that of the degraded wetlands in the Mississippi River Delta. Although the tidal flat wetlands have a lower carbon sequestration per unit area, their widespread distribution and rapid sedimentation make them among the highest in carbon burial efficiency per unit area globally.

The YRD is dominated by the Phragmites australis, Suaeda salsa, and Tamarix chinensis communities, whose root exudates and litter inputs significantly enhance the stability of SOC. In contrast, the Mississippi River Delta is primarily dominated by flood-tolerant herbaceous plants. After vegetation loss, the soil redox potential declines, accelerating microbial decomposition rates and resulting in carbon loss [36]. Similarly, the Yangtze River Delta experiences reduced carbon input due to artificial wetlands and urbanization, with soil carbon stability lower than that of natural wetlands [37,38]. In contrast, the Mississippi River Delta experiences insufficient sedimentation, and subsidence has become the primary driver of carbon loss. Unlike the Yangtze River Delta and the Mississippi River Delta, the carbon sink function of the YRD heavily relies on natural sedimentation processes.

Vegetation types significantly regulate SOC accumulation through variations in biomass allocation, root architecture, and litter input traits [39]. In the YRD, the SOC content in Phragmites australis community was significantly higher than in the Suaeda salsa and Tamarix chinensis communities, primarily attributed to the former’s superior photosynthetic carbon assimilation, well-developed rhizome systems, and deep-root biomass [40]. The annual organic carbon input from litter and root exudates in Phragmites australis is relatively high, whereas Suaeda salsa and Tamarix chinensis exhibit reduced carbon input due to high lignin/nitrogen ratios in litter and shallow-root distribution [41].

Vegetation type, as a key biological driver, interacts with geographical topography and water–salt conditions to form a multi-scale mechanism governing SOC spatial differentiation [42]. Across all vegetation types, the highest SOC content occurred in the surface soil layer [43], consistent with global observations. This phenomenon is likely driven by surface litter coverage, where warmer and moister microconditions in the 0–20 cm layer enhance litter decomposition efficiency compared to in deeper soils. Gill et al. further reported that peak litter decomposition rates occur at a 10–15 cm depth [44], which stimulates microbial activity by increasing soil nutrient availability. This highlights the pivotal role of microbial communities in mediating SOC cycling and accumulation [45].

DOC originates primarily from plant residue leaching, SOC hydrolysis, root exudation, and microbial metabolites. In this study, the spring DOC content correlated significantly with electrical conductivity (EC, p < 0.05), whereas autumn DOC exhibited a highly significant association with soil moisture (p < 0.01). This sensitivity is driven by DOC’s rapid response to environmental fluctuations, such as tidal regimes and exogenous carbon inputs [46]. Jin et al. further demonstrated that EC influences soil colloidal properties, thereby regulating DOC dynamics [47]. This mechanism is consistent with our findings. While previous research reports a universal positive correlation between SOC and DOC [48,49], this study observed a seasonal dissociation: no significant spring correlation yet a strong autumn association (p < 0.01). This discrepancy stems from the complex, season-dependent sources of soluble organic carbon [50]. Specifically, the paradoxical spring DOC peak in the Suaeda salsa community, despite low SOC, highlights the microbial mediation of carbon mobilization. Spring rains likely triggered the osmotic release of labile carbon from salt-stressed microbial communities, while autumn floods promoted DOC loss via lateral leaching, decoupling microbial activity from carbon retention. Such hydrological perturbations underscore the vulnerability of deltaic carbon stocks to extreme climate events, as transient environmental shifts can disrupt the equilibrium between carbon supply, microbial processing, and storage [51].

4.2. Effects of Soil Microbial Communities on Wetland SOC

Wetlands function as critical hotspots for carbon and nitrogen cycling, playing a pivotal role in global climate regulation and ecosystem homeostasis [52]. Across seasons, Proteobacteria dominated the spring and autumn soil microbial communities, consistent with their well-documented roles in organic matter decomposition and microbial nitrogen fixation/desulfurization processes [53]. In autumn, Firmicutes emerged as a co-dominant phylum alongside Proteobacteria. This phylum is influenced by the soil pH, clay content, C/N ratio, and altitude, with genera like Bacillus and Clostridium driving key steps in carbon transformation [54]. Spring soils exhibited higher α-diversity (ACE, Chao1), particularly in the deep layers of the Phragmites australis community, which correlated with an increased organic matter decomposition potential during the plant growing season. The spring dominance of Proteobacteria and Desulfobacterota aligns with their roles as versatile heterotrophs degrading labile carbon substrates. Conversely, autumn’s reduced richness but increased Shannon index coincided with diminished SOC mineralization, as declining temperatures suppressed microbial activity and favored carbon retention. Notably, the shallow-rooted Suaeda salsa community displayed minimal vertical diversity gradients, mirroring its limited SOC stratification, whereas the Phragmites australis and Tamarix chinensis communities exhibited depth-dependent microbial zonation that facilitated SOC accumulation in subsurface layers.

Across seasons, Gammaproteobacteria and Alphaproteobacteria were the dominant classes, with Betaproteobacteria absent from the dominant taxa. This contrasts with Chen et al.’s findings, which showed an increase in Betaproteobacteria along freshwater-to-hypersaline gradients in wetlands [55]. Gammaproteobacteria include chemolithoautotrophic and photolithoautotrophic sulfur-oxidizing bacteria, which degrade hydrocarbons and mediate nitrogen transformations under saline conditions, highlighting their role in saline wetland biogeochemistry. Zada et al. discovered high-pressure-tolerant urease-producing bacteria in methane hydrate sediments, further demonstrating the critical role of microorganisms in wetland carbon cycling [56]. This finding highlights the adaptability of microbial communities to extreme environments and their functional significance in biogeochemical processes. Deltaproteobacteria showed elevated autumn abundances, occupying both saline and freshwater niches as key participants in sulfur cycling. Genera such as Desulfosarcina, Desulfobulbus, and Desulfurococcus are critical for anaerobic methane oxidation in wetland sediments. Bacteroidota degrade environmental polymers, while Actinobacteriota and Firmicutes facilitate the decomposition of complex organic matter, underscoring their indispensability for wetland bioremediation and carbon turnover [57].

The seasonal dynamics of wetland microbial communities and their synergistic interactions with vegetation types are key mechanisms regulating carbon sequestration potential [58,59]. In spring, dominant phyla, such as Proteobacteria, rapidly decompose and assimilate organic matter for short-term carbon capture, while in autumn, newly introduced phyla, such as Firmicutes and Halobacteria, shift towards long-term carbon sequestration through detritus accumulation and mineral interactions. In the Phragmites australis community, high microbial diversity and root penetration create a positive carbon sink cycle characterized by “rapid turnover–stable sequestration”. In contrast, in the Tamarix chinensis community, salt stress induces microbial functional convergence, with carbon sequestration primarily based on short-term detritus accumulation but with a risk of carbon loss induced by high salinity. The coupling of sulfur cycling with microbial processes further strengthens the stability of long-term carbon pools [60]. Seasonal transitions drive the reorganization of microbial community structures, establishing a dynamic equilibrium in carbon pools.

Clustering analysis revealed distinct vegetation-specific microbial guilds. The Phragmites australis community formed a unique cluster enriched in Proteobacteria and Bacteroidota, which are taxa specialized in utilizing labile rhizodeposits. In contrast, the Tamarix chinensis and Suaeda salsa communities selected for Desulfobacterota and Halobacteriaota, microbial lineages adapted to saline, waterlogged microhabitats. These niche-based assemblies established divergent carbon cycling hotspots: the Phragmites australis community promotes continuous humification via high-quality litter inputs and rhizosphere stimulation, whereas the Tamarix chinensis and Suaeda salsa communities favor short-term carbon storage in microbial biomass or anaerobic byproducts [61]. Vegetation growth enhances microbial diversity and soil nutrient availability, illustrating a strong linkage between plant activity and the structural diversity of soil microbial communities [62]. This plant–microbe interdependence suggests that fostering plant-associated mutualistic microbes, such as those enriched in Phragmites australis rhizospheres, could serve as a targeted strategy for restoring degraded coastal wetlands in the YRD [63].

The interaction between microorganisms and plants forms a core feedback loop in wetland ecosystems, where root exudates drive community assembly, and microbial metabolic products regulate plant growth. This provides a carbon source for soil microorganisms, participates in the carbon cycle, influences dynamic changes in SOC, and thus impacts the dynamic balance of the wetland ecosystem’s carbon pool [64]. In the YRD wetlands, this mechanism significantly influences vegetation adaptability and carbon sequestration pathways. For example, during the growing season (spring), the roots of Phragmites australis plants secrete low-molecular-weight organic acids and flavonoids, enriching nitrogen-fixing bacteria and phosphate-solubilizing bacteria from the phylum Proteobacteria, with their abundance 30–40% higher than in non-rhizosphere soils. These microorganisms promote Phragmites australis root expansion by synthesizing indole-3-acetic acid (IAA), forming a positive feedback loop of “plants promote microbes—microbes promote plants [65]”. Meanwhile, under salt stress, Tamarix chinensis secretes osmotic regulators that induce the colonization of halophilic bacteria from the phyla Halobacterota and Firmicutes, helping the plant maintain cellular osmotic pressure while degrading litter and releasing bioavailable carbon. Additionally, Desulfobacterota reduces sulfate to sulfides, which then combine with sodium ions in the soil to form sodium sulfide precipitates, thereby lowering rhizosphere salinity and mitigating the toxic effects of sodium ions on plant roots. The microbe–plant feedback mechanism enhances both vegetation adaptability and carbon cycling efficiency through the coordination of chemical signaling, metabolic product exchanges, and stress responses. It is worth noting that heavy metals disrupt microbial cell membrane integrity, interfere with enzyme activity, and damage genetic material, leading to declines in microbial community diversity and reductions in functional redundancy [66]. For example, high concentrations of Cd pollution significantly suppress the abundance of Proteobacteria and Acidobacteria in soil, while promoting the enrichment of metal-resistant bacteria, such as Bacillus [67]. However, plants form specific microecological systems through root exudates and symbiotic microorganisms, mitigating heavy-metal toxicity and regulating carbon dynamics [68]. By leveraging these synergistic interactions, bioremediation efforts may enhance soil carbon sequestration, nutrient cycling, and ecosystem resilience, highlighting the translational potential of microbe–plant feedback mechanisms in wetland restoration frameworks.

4.3. Interactions Among Plants, Soil Environment, and Soil Microbes

This study identified EC as a key environmental driver in both spring and autumn. While EC reflects the total soil salt content, the effect of salinity on bacteria within the same taxonomic group varied significantly between seasons. Microbial diversity displayed divergent response mechanisms to salt fluctuations, with no monotonic relationship observed between diversity indices and soil salinity [69]. In coastal wetlands, soil salinity is influenced by seawater immersion duration and hydrological dynamics, directly shaping microbial community composition [70]. Thus, tidal regimes likely serve as a pivotal driver of bacterial diversity and community structure variations in the YRD [71].

RDA identified SOC and TN as key environmental factors shaping microbial community structure. Gammaproteobacteria exhibited a significant positive correlation with SOC and TN, indicating their enrichment in carbon-rich and nitrogen-rich habitats. Similarly, Desulfuromonadia, Bacteroidia, and other taxonomic groups were also positively correlated with SOC and TN. Collectively, these results suggest that carbon and nitrogen availability act as core drivers of microbial community composition. Carbon-rich and nitrogen-rich environments likely provide abundant energy substrates and nutrients, facilitating the growth and proliferation of associated microbial taxa [72]. Desulfobulbia was positively linked to EC, whereas Acidobacteria displayed negative correlations with EC, DOC, and other factors, highlighting diverse microbial adaptation strategies to ion concentrations and labile carbon availability. Nitrososphaeria had a positive association with DOC, while Campylobacteriad and Alphaproteobacteria were closely correlated with DOC and TP. These relationships imply that the metabolic activities of these microorganisms may depend on the availability of DOC and phosphorus, reflecting their specific nutrient requirements [73].

RDA further revealed both conserved microbial compositional patterns across soil area and divergent taxon–environment relationships, indicative of niche differentiation among microbial groups. For example, Gammaproteobacteria and Bacteroidia, taxa exhibiting strong affinities for labile carbon–nitrogen substrates, dominated in nutrient-rich environments, whereas lineages like Acidobacteriota displayed negative associations with carbon–nitrogen gradients, suggesting preferential adaptation to oligotrophic or specialized physicochemical niches. This niche partitioning minimizes interspecific competition, thereby sustaining microbial community stability and diversity. Microbial diversity showed scale-dependent drivers: at the micro-scale, plant roots served as key determinants by creating heterogeneous microhabitats through adjustments in the soil pore structure, the provision of low-molecular-weight root exudates, and the modulation of redox potential and pH, which selectively enriched beneficial taxa. At the macro-scale, however, microbial diversity was shaped by broader environmental gradients and spatial processes, as documented in previous studies [74]. This dual-scale influence underscores the intricate interplay between local plant–microbe feedbacks and regional environmental filters in structuring wetland microbial communities.

CLQ series samples clustered closely with Desulfobacteria, indicating that higher pH values promote the enrichment of this taxon, likely due to their physiological adaptation to alkaline conditions. LWQ series samples exhibited strong associations with SOC and TN, suggesting elevated carbon–nitrogen availability in their microhabitats and corroborating the filtering effect of environmental gradients on microbial community assembly.

Seasonal differences in soil microbial community composition were primarily driven by variations in soil physicochemical properties and vegetation cover. Among these drivers, carbon–nitrogen nutrients emerged as dominant factors shaping microbial community assembly [75], whereas EC, pH, and DOC influenced the community structure by modulating microbial osmoregulation, enzyme activity, and labile carbon acquisition. Given the tight coupling between vegetation, environmental factors, and the microbial community structure, nutrient elements like Na, P, and K may act as critical limiting factors for wetland soil microbial growth and activity. Further research is needed to dissect their roles in microbe-mediated biogeochemical cycles, specifically how ion balance and nutrient stoichiometry influence microbial functional guilds and carbon–nitrogen–sulfur coupling processes in coastal wetland ecosystems.

5. Conclusions

This study reveals the spatiotemporal variations in SOC and microbial-driven mechanisms in the YRD. The results indicate that different vegetation types significantly affect the SOC content, with the sequence being Phragmites australis > Suaeda salsa > Tamarix chinensis. The seasonal dynamics of DOC are regulated by environmental factors, highlighting the influence of tidal action and exogenous carbon input on the active carbon pool. Microbial community analysis shows that Proteobacteria are the dominant phylum, involved in organic matter decomposition, sulfur cycling, and anaerobic methane oxidation processes. Desulfobacteria drive carbon–sulfur coupled metabolism through sulfate reduction, while Bacteroidetes and Firmicutes dominate the degradation of complex organic matter. The vegetation type regulates microbial diversity by altering root exudates and the soil microenvironment, while the EC, pH, and nutrient elements are key environmental factors driving the spatiotemporal differentiation of microbial communities. Moreover, the seasonal correlation differences between SOC and DOC suggest that the pathways of organic carbon transformation are influenced by the complex interactions of multiple factors, such as temperature, moisture, and microbial activity.

Wetland restoration should focus on microbial communities, integrating vegetation management, seasonal regulation, and technological innovation to establish a “rapid turnover–stable sequestration” carbon sink system. Inthe Phragmites australis community, the focus should be on protecting the functional roles of microbial communities, ensuring an anaerobic microenvironment for reed roots through ecological water supplementation, promoting functional interactions between the phyla Proteobacteria and Desulfobacterota, and enhancing the sulfate-reduction-driven coupling process of carbon mineralization and sequestration. Simultaneously, retaining some litter cover in autumn and promoting microbial functional redundancy through root exudate diversity can enhance the resilience of the carbon sink across seasons. In high-salinity environments, particularly in areas dominated by the Suaeda salsa and Tamarix chinensis communities, it is necessary to enhance carbon storage resilience through salt gradient restoration and microbial inoculation. Future studies should combine long-term observational data to analyze the synergistic response mechanisms of the “plant-microbe-carbon cycle” under multi-scale environmental stressors.