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Article

Changes in Community Structure and Functional Characteristics of Soil Bacteria and Fungi along Karst Vegetation Succession

by
Yuanyong Li
1,2,
Qian Tang
3,
Congjun Yuan
2,
Sixi Zhu
3,
Yuyan Ye
1,2,
Peng Wu
2,4,
Yingchun Cui
2 and
Fangjun Ding
2,4,*
1
Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-Bioengineering, Guizhou University, Guiyang 550025, China
2
Guizhou Academy of Forestry, Guiyang 550005, China
3
College of Eco-Environmental Engineering, Guizhou Minzu University, Guiyang 550025, China
4
Guizhou Libo Observation and Research Station for Karst Forest Ecosystem, Libo 558400, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(8), 1562; https://doi.org/10.3390/f14081562
Submission received: 29 May 2023 / Revised: 29 June 2023 / Accepted: 29 July 2023 / Published: 31 July 2023
(This article belongs to the Section Forest Soil)
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Abstract

:
Soil microbes are a crucial component of karst ecosystems, and exploring their community changes during succession can help to elucidate the mechanisms driving succession dynamics. However, the variation of soil microbial communities during vegetation succession in karst ecosystems is still poorly understood. We studied the variations in community structure and potential functions of soil microbes within the four successional stages of grassland (GL), shrubland (SL), secondary forest (SF), and primary forest (PF) for the topsoil (0–10 cm) and subsoil (10–20 cm) in a karst area using high-throughput sequencing. The research findings showed that the bacterial and fungal community diversity and composition changed more obviously in the topsoil than in the subsoil across the succession. With vegetation succession, the structural and functional characteristics of soil bacterial and fungal communities show different trends, with soil fungal communities having a greater response to successional stage changes. Actinobacteria and Acidobacteria were dominant in secondary and primary forests, respectively, while Bacteroidetes was prevalent in grassland. However, the change in Proteobacteria was not significant at both soil depths. Ascomycota was the dominant phylum of soil fungi throughout the succession. The function of soil bacteria was mainly carbohydrate metabolism, which had the highest proportion in the shrubland at different soil depths. The dominant fungal functional groups were saprotroph, pathotroph, and pathotroph–saprotroph. The soil bacterial communities were observably affected by soil organic carbon, total nitrogen, total potassium, ammonia nitrogen, nitrate nitrogen, and leucine aminopeptidase, among which soil organic carbon, ammonia nitrogen, and leucine aminopeptidase mainly influenced the bacterial community in the topsoil, while nitrate nitrogen chiefly influenced the bacterial community in the subsoil. The soil fungal community was only significantly affected by soil organic carbon. Collectively, these results indicate that the effects of vegetation succession on soil microbial communities are largely driven by successional stage and soil properties, with soil fungi being more susceptible to the vegetation successional stage and soil bacteria being more sensitive to the soil properties. During this process, soil bacterial and fungal communities follow different succession patterns.

1. Introduction

Vegetation succession not only alters the surface landscape but also alters the circulation of materials and the transformation of energy in soil ecosystems and has a profound impact on soil microorganisms’ diversity, composition, and function [1,2,3]. Soil bacteria and fungi communities comprise a relatively high proportion of soil microbial communities, which are highly sensitive to external environmental changes and may be affected by vegetation succession [4,5]. Ren et al. concluded that the soil bacterial community dominated the early vegetation successional stage, while the soil fungal community dominated the late vegetation successional stage [6]. Zhang et al. observed that the soil fungal community changed more synchronously with the plant community succession, but the soil bacterial community had no noticeable variation [7]. Jiang et al. found that the vegetation succession dramatically affected the fungal functional diversity but did not significantly affect the bacterial functional diversity [2]. Even though previous research has shown that the succession of vegetation communities may lead to changes in soil microorganisms [8], there is still room for further improvement in studying the change rules of soil bacterial and fungal communities during vegetation succession.
As the primary driver of soil nutrient conversion and carbon metabolism, soil microbial groups play a vital role in regulating the ecosystem’s carbon and nitrogen cycles by decomposing various organic residues [9]. In microbial ecology, soil microorganisms can be classified into the copiotrophic category or oligotrophic category, depending on their growth rate and nutrient utilization capacity [10,11,12]. Some studies have suggested that the copiotrophic category corresponds to the r-strategy, whereas the oligotrophic category corresponds to the k-strategy [13,14]. Generally speaking, a soil bacterial community (r-strategy) inclined to a nutrient-rich environment grows fast in the early succession stages. In contrast, soil fungal communities (k-strategy) have a strong nutrient competition ability present more commonly in the late succession stages [15,16].
Soil microorganisms are easily disturbed by the external environment, and their diversity, composition, and function vary in response to environmental changes [17,18,19]. There are various momentous factors affecting soil microbes, including the soil pH, texture, and nutrient levels [20,21]. Moreover, some microbes are observably affected by soil enzymes [22]. Soil pH is the critical element changing the structure and functional groups of soil microbial communities along the vegetation succession [17,23], and soil organic carbon, total nitrogen, and total phosphorus are equally influential elements in determining soil microbial community changes [24,25]. Due to the high-nutrient requirement during the succession process, the sensitivity to soil nutrients of the soil bacterial community was higher than that of the soil fungal community, according to Zhu et al. [12]. Of course, the reactions in soil microbial communities to soil properties can also reveal soil qualities and the nutrient status. Soil ecosystem functions are closely related to soil microbial communities [26,27,28]. Bacterial community diversity reduction may cause a loss in the multifunctionality resistance and productivity of soil ecosystems [29]. The fungal community structure affects nutrient transport and conversion in the forest ecosystem [30]. Therefore, soil microbial communities can be regarded as significant indicators reflecting the soil quality and ecological function. It is of great importance to study their adaptive strategies and functional changes to environmental changes for the health and stability of soil ecosystems.
As a unique ecological environment system, karst ecosystems maintain an abundant soil microbial diversity. Maolan National Nature Reserve, Guizhou Province, China, is currently the largest area of karst native forest distribution at the same latitude region in the world and has great research value. In addition, this area is a fragile karst ecological zone with broken terrain, a shallow soil layer, and numerous habitat types, which is a good representative of the whole karst area. At present, the dynamics in the vegetation structure and soil properties across the succession are currently a popular topic for research in this region [31,32]. Nevertheless, few studies have been conducted on microbial community variations in both soil depths following karst vegetation succession. Our study focuses on the changes in the structure and function of soil bacterial and fungal communities in the karst ecosystem of Maolan. This study area provides a unique location for studying bacterial and fungal community succession patterns, with a variety of vegetation types, such as grassland, shrubland, secondary forest, and primary forest [20,33]. This research was conducted to (1) clarify the succession patterns of soil bacterial and fungal communities; (2) explore the changes in diversity, composition, and function of soil bacterial and fungal communities at both soil depths across the succession; and (3) analyze the pivotal elements influencing the changes in the soil microbial community.

2. Materials and Methods

2.1. Study Region and Soil Sample Gathering

The study was carried out in Maolan Karst National Nature Reserve in Southwest China’s Guizhou Province (107°52.2′–108°5.7′ E, 25°9.3′–25°20.8′ N) (Figure 1). The landform is dominated by peak forests and peak cluster depressions, with an average elevation of 550–850 m. This region possesses a humid mid-subtropical monsoon climate with a mean annual temperature of 15.3 °C and a mean annual relative humidity of 83.0%. The mean annual precipitation is 1752.5 mm, mainly from June to September [34]. The parent rocks are primarily pure limestone and dolomite, and the soils are mostly black lime soils. The vegetation cover of evergreen and deciduous broad-leaved mixed forests is 88.6% [35]. Representative vegetation types mainly cover the grassland, shrubland, and secondary and primary forests. More detailed land information on the vegetation at the successional sites is presented in Table S1.
Soil sample collection was conducted in May 2019. Three similar sample plots (30 m × 30 m) were set up at different vegetation successional types. In each sample plot, three sampling points were selected, and a square (2 m × 2 m) was painted around each sampling point. Each square collected five soil samples from the topsoil and subsoil, respectively, and were then blended at the same depth to make one mixed sample. Each vegetation type at the two soil depths was collected in eighteen mixed samples, totaling seventy-two composite soil samples. After removing plant and animal residues and small stones, each mixed soil sample was split into three subsamples. One subsample was air-dried to detect the soil properties, and the other two were refrigerated for the extraction and sequencing of DNA and soil enzyme activity determination.

2.2. Soil Properties and Enzymatic Activity Determination

The pH meter was used to determine the soil pH in the soil-to-water ratio suspension 1:2.5. The H2SO4-K2Cr2O7 method was used to measure the soil organic carbon (SOC) [36]. The H2SO4-H2O2 digestion method was used to determine the total nitrogen (TN) [2]. The determination of the ammonia nitrogen (NH4+-N) and nitrate nitrogen (NO3−-N) contents were extracted with potassium chloride solution and then detected by an autoanalyzer (AA3, Bran-Luebbe, Hamburg, Germany) [2]. The molybdenum blue colorimetric method was used to analyze the total phosphorus (TP) [37]. The soil available phosphorus (AP) was colorimetrically measured at 700 nm [37]. The detection processes of leucine aminopeptidase (Leu), acetylglucosaminidase (Ace), and glucosidase (Glu) were as follows: reaction wells, inorganic control wells, substrate wells, and blank control wells were set up, respectively, and four replicates were set up. The soil samples’ shaking solution and buffer solution in different proportions were added to a 96-position black enzyme-labeled plate, incubated at 37 °C or 25 °C for 4 h, and then subjected to fluorescence measurements using the multifunctional fluorescent enzyme-labeled instrument (Synergy H1, BioTek, Winooski, VT, USA), with excitation at 365 nm and the detection of fluorescence at 450 nm [38].

2.3. DNA Extraction and High-Throughput Sequencing

According to the manufacturer’s instructions, the total genomic DNA samples in the soil were abstracted using the OMEGA Soil DNA Kit (D5625-01) (Omega Bio-Tek, Norcross, GA, USA). Nanodrop NC-2000 (Thermo Fisher Scientific, Waltham, MA, USA) and agarose gel electrophoresis (Beijing Liuyi, DYY-6C, Beijing, China) were used to detect the concentration and purity of the extracted DNA. The V3-V4 region of the bacterial 16S rRNA was amplified by the primers 338F (5’-ACTCCTACGGGAGGCAGCAG-3’) and 806R (5’-GGACTACHVGGGTWTCTAAT-3’) [39]. The ITS1 region of fungi was amplified by the primers ITS1F (5’-CTTGGTCATTTAGAGGAAGTAA-3’) and ITS2R (5’-GCTGCGTTCTTCATCGATGC-3’) [40]. The primary process of amplification was pre-denaturation at 95 °C for 3 min, followed by 27 cycles of amplification (95 °C for 30 s, 55 °C for 30 s, and 72 °C for 30 s), and then stable extension at 72 °C for 10 min. Ultimately, the PCR products were sent to Illumina’s MiSeq platform at Shanghai Majorbio Bio-pharm Technology Co., Ltd. Shanghai, China, where the database construction and sequencing work were completed. The quality of the original sequencing sequences was controlled by FASTP to ensure the dependability and authenticity of the data. Based on the overlapping relationship between PE reads, FLASH was used to splice the reads of each sample to obtain valid data. UPARSE was used to perform OTU clustering on sequences based on 97% similarity and remove single sequences and chimeras during the clustering process. Each sequence was annotated with an RDP classifier for species classification, with the bacterial community using the Silva database and fungal community using the Unite database. The functions of the bacterial and fungal communities were forecast by Tax4Fun and FUNGuild, respectively [41,42].

2.4. Data Analyses

The preliminary data processing was carried out using Microsoft Excel 2022 and SPSS 23.0. One-way analysis of variance (ANOVA) was applied to analyze the differences in the soil properties and soil microbial characteristics among the four succession stages [43]. The relation between the soil properties and the diversity of the microbes was analyzed by Pearson’s correlation. Based on the Bray–Curtis distance, a principal coordinate analysis (PCoA) was used to examine the microbial community and functional structure. The differences in the microbial communities were detected by an analysis of similarity (ANOSIM) [44]. The relationship between the soil factors and microbial community composition was analyzed using a redundancy analysis (RDA). Furthermore, the relationship between the soil factors and soil microbial phyla was investigated using a Spearman correlation analysis.

3. Results

3.1. Soil Properties in Different Vegetation Successional Stages

During vegetation succession, the soil properties were altered dramatically at two depths (Table 1). The total nitrogen (TN), ammonia nitrogen (NH4+-N), and nitrate nitrogen (NO3−-N) contents followed the same change trend at both soil depths and increased significantly from grassland to primary forest (p < 0.05). At the depths of 0–10 and 10–20 cm, the contents of soil organic carbon (SOC) and total phosphorus (TP) had the highest values in primary forest and shrubland, respectively, and the lowest values in grassland (p < 0.05). The leucine aminopeptidase (Leu), acetylglucosaminidase (Ace), and glucosidase (Glu) contents at the two soil depths firstly increased and then decreased following the vegetation succession. The Leu, Ace, and Glu contents were higher in shrubland than in the other stages of succession (p < 0.05). Moreover, the pH and available phosphorus (AP) at both soil depths did not show significant changes over the succession (p > 0.05). The above results indicated that the soil properties of the two soil depths exhibited different trends at the four vegetation successional stages.

3.2. Soil Microbial Community Diversity and Composition in Different Vegetation Successional Stages

The soil bacterial and fungal community diversity indexes varied across various successional stages at the two depths, but the directions were inconsistent (Figure 2). The bacterial Shannon index and Chao1 index decreased observably from grassland to the primary forest at the 0–10 cm depth (p < 0.05) (Figure 2A,C). At a depth of 10–20 cm, the soil bacterial Shannon index and Chao1 index showed a trend of increasing first and then decreasing in the different successional stages. Still, the changes were not noteworthy (p > 0.05) (Figure 2B,D). The Shannon index and Chao1 index of soil fungi at both soil depths first increased and then reduced during the succession, with the highest values in the secondary forest (Figure 2E–H). The fungal Shannon index at the 10–20 cm depth and Chao1 index at both depths did not differ markedly among the different successional stages of vegetation (p > 0.05) (Figure 2F–H). The principal coordinate analysis (PCoA) results indicated that the community structures of bacteria and fungi at the two soil depths were separated during the four different stages (Figure 3). Furthermore, the results of the ANOSIM tests (Bray–Curtis distance) also revealed that the bacterial communities at both soil depths were substantially distinct between any two vegetation stages, except for the secondary and primary forests at the 10–20 cm depth (Table S2). In contrast, significant changes in the fungal community occurred at the different vegetation succession stages at the two soil depths (Table S2). These results suggested that the vegetation succession not only affected the diversity of the soil bacterial and fungal communities but also had a significant impact on their community structures.
The main phyla of bacteria with a relative abundance greater than 1% at the two depths in the various vegetation succession stages were Proteobacteria (29.7%~34.1%), Acidobacteria (12.7%~19.5%), Actinobacteria (11.4%~20.6%), Chloroflexi (6.9%~12.5%), Nitrospirae (4.0%~11.5%), Verrucomicrobia (2.2%~7.7%), Bacteroidetes (1.0%~5.3%), Planctomycetes (1.9%~3.5%), Latescibacteria (1.1%~1.9%), Tectomicrobia (1.1%~1.8%), Gemmatimonadetes (1.0%~1.8%), and Firmicutes (0.9%~6.7%) (Figure 4A,B). The response of Proteobacteria to the vegetation succession at the two soil depths showed different trends, but their responses had no noteworthy changes (p > 0.05) (Figure 4A,B). Acidobacteria and Actinobacteria at both depths were dominant in secondary and primary forests, respectively, while Bacteroidetes were commonly present in grassland (Figure 4A,B). Meanwhile, Chloroflexi, Nitrospirae, and Verrucomicrobia had significant differences at both depths among all the vegetation stages (Figure 4A,B). For fungi, Ascomycota (37.9%~61.4%) was the dominant fungal phyla, whereas Basidiomycota (8.7%~28.0%), Mortierellomycota (8.6%~30.0%), and Rozellomycota (0.1%~5.5%) were the main fungal phyla (Figure 4C,D). At the 0–10 cm depth, the relative abundance of Ascomycota and Rozellomycota increased dramatically in the secondary and primary forests (p < 0.05) (Figure 4C). The grassland had a greater relative abundance of Basidiomycota than the primary forest, secondary forest, and shrubland (p < 0.05) (Figure 4C). Mortierellomycota at the two depths was increased in the shrubland (p > 0.05) (Figure 4C). Along the vegetation succession, there was no significant change in the main fungal phyla at the 10–20 cm depth (Figure 4D). In addition, the ratio of fungi to bacteria increased substantially at a depth of 0–10 cm (p < 0.05) but not at a depth of 10–20 cm (p > 0.05) with the vegetation succession (Figure 4E,F). In conclusion, during the succession, not only the soil bacterial and fungal communities but some dominant bacterial and fungal phyla did not follow the same succession patterns.

3.3. Soil Microbial Community Function in Different Vegetation Successional Stages

The sequences acquired from 16S data were annotated into the KEGG database to study the impacts of vegetation succession on the bacterial functional diversity at the two soil depths. Forty-one functional categories were detected with a carbohydrate metabolism (12.67%~12.97% of the total predicted genes) of the highest abundance, which mainly dominated in shrubland at both soil depths (Figure 5). Across all the vegetation succession stages, the energy metabolism, metabolism of cofactors and vitamins, and translation and metabolism of terpenoids and polyketides showed significantly increasing trends at the two depths, whereas nucleotide metabolism in both soil depths was markedly decreased (Figure 5). The trophic patterns of the fungal communities were divided into seven categories according to the FUNGuild database: pathotroph, saprotroph, symbiotroph, pathotroph–saprotroph, pathotroph–symbiotroph, saprotroph–symbiotroph, and pathotroph–saprotroph–symbiotroph (Figure 6). Pathotroph and saprotroph increased at both depths during vegetation succession, and these modes were enriched in the secondary forest (Figure 6). The pathotroph–saprotroph relative abundance in shrubland was higher than in the primary forest, secondary forest, and grassland (Figure 6). Symbiotroph and pathotroph–symbiotroph did not change dramatically at both soil depths among the four successional stages (Figure 6). We further used a PCoA analysis to explore the soil microbial community’s functional structure. Like the structure of the microbial community, the soil microbial community’s functional structure varied markedly in different vegetation types at the two depths (Figure S1). Collectively, there were differences in the functional groups of the soil bacterial and fungal communities at the two soil depths in the different successional stages.

3.4. The Correlation between Soil Microbial Communities and Soil Properties

The soil properties were closely related to the community composition of the soil microorganisms. According to the redundancy analysis (RDA) findings, all soil properties interpreted 42.8% and 26.1% of the relation between the soil bacterial community and soil properties in the topsoil and subsoil, respectively (Figure 7A,B). At the 0–10 cm soil depth, the SOC (p = 0.001), TN (p = 0.001), TP (p = 0.001), NH4+-N (p = 0.001), and leu (p = 0.004) markedly influenced the soil bacterial community changes (Figure 7A). Among them, the SOC, TN, TP, and NH4+-N showed a significantly positive association with Nitrospirae (p < 0.05) and a significantly negative correlation with Chloroflexi and Verrucomicrobia (p < 0.05) (Figure S2). The soil leu was mainly associated with Proteobacteria, Acidobacteria, Verrucomicrobia, and Gemmatimonadete (p < 0.05) (Figure S2). The soil TN (p = 0.022), TP (p = 0.003), and NO3−-N (p = 0.043) were the crucial factors influencing the changes in the soil bacterial community at the 10–20 cm depth (Figure 7B). The TN and TP in the soil were positively associated with Actinobacteria and Nitrospirae (p < 0.05) but negatively associated with Chloroflexi and Verrucomicrobia (p < 0.05) (Figure S2). Additionally, NO3−-N played an important role in promoting the development of Acidobacteria, Nitrospirae, and Latescibacteria (p < 0.05) but inhibited the growth of Proteobacteria (p < 0.05) (Figure S2). All the soil properties interpreted 20.3% and 32.3% of the relationship between the soil fungal community and soil properties in the topsoil and subsoil, respectively (Figure 7C,D). At the 0–10 cm depth, the SOC (p = 0.008) markedly influenced the soil fungal communities, which had a significantly positive association with Ascomycota and Mortierellomycota (p < 0.05) and a significantly negative association with Basidiomycota (p < 0.05) (Figure 7C and Figure S3). In contrast, the soil properties had no significant effect on the soil fungal community at the 10–20 cm depth (p > 0.05) (Figure 7D). These results showed that, compared to soil fungi, soil bacteria are more susceptible to soil properties.

4. Discussion

4.1. Changes in Soil Microbial Community Diversity during Vegetation Succession

The diversity of soil microbes is an important index for evaluating ecosystem functions [26]. Previous studies have demonstrated that variations in a vegetation community may lead to changes in the soil properties, especially in the topsoil, resulting in bacterial and fungal community diversity differences [20,45,46]. We found that the soil bacterial diversity decreased in the two depths following the vegetation succession, whereas the fungal diversity increased initially and then decreased (Figure 2). One of the main reasons might be correlated with soil bacterial and fungal community niches [10]. It has been demonstrated by several previous studies that soil bacterial communities with a high turnover rate primarily dominate in the early succession stage, whereas soil fungal communities with a low turnover rate mainly dominate in the late succession stage [6,12]. The different changes in bacterial and fungal community diversity over a succession may also be attributed to the adaptability to soil factors [2,24]. In our study, the fungal community diversity was positively associated with the SOC and TN at two different depths of the soil (p < 0.05) (Table S3). In the forest stages, the higher SOC and TN concentrations might have increased the soil fungal diversity. Conversely, our research demonstrated that the diversity of the soil bacterial communities was negatively or insignificantly correlated with the SOC and TN in the topsoil and subsoil, respectively (Table S3), which might have reduced the diversity of the bacterial communities along the vegetation succession. The soil pH is also considered a vital factor in predicting the diversity of bacterial communities [17,21,47]. However, our study found no significant association between the bacterial community diversity and pH value (Table S3). However, the impact of pH on a soil bacterial community cannot be neglected, as the decrease in pH will inhibit bacterial growth and reduce bacterial diversity during successions in our study area [12,48]. Compared with the secondary forest, the primary forest had lower plant species in a karst region, which might be related to the interspecific competition among the plants [49]. The soil fungi communities were closely related to the plant species. Hence, this could explain why the diversity of fungal communities declines in primary forests [50].
The PCoA and ANOSIM analyses demonstrated that the bacterial and fungal community structures altered dramatically at both depths along the succession, and the fungal community structure variation was stronger than the bacterial community (Figure 3 and Table S2), which agreed with the results of Jiang et al. [2]. Soil fungi establish a biological nutritional relationship with plants through the formation of mycorrhizas, root nodules, and other symbiotic systems [19]. This can explain why fungal communities are sensitive to different vegetation habitat changes. Bacterial community changes are also related to vegetation changes, which is more likely due to soil property variations induced by vegetation changes [18]. Taken together, the bacterial and fungal community diversities and structures at two depths presented differential responses to the four vegetation succession stages.

4.2. Changes in Soil Microbial Community Composition during Vegetation Succession

Vegetation alters soil nutrients by changing the litter input and root exudates and thus leads to a change in the community composition of soil microbes [19,24]. Our research found that the ratio of fungi to bacteria increased observably during the vegetation succession at the 0–10 cm depth (p < 0.05) (Figure 4E), while it did not change observably at the 10–20 cm depth (p > 0.05) (Figure 4F). This suggested that the changes in the niche of the bacterial and fungal communities were more significant in the topsoil than in the subsoil under the different successional stages [20]. Following the succession of vegetation, the increase in the fungal community’s niche occupied the bacterial community’s niche [17,45]. Regarding the bacterial community composition, from the grassland to the forest stages, Bacteroidetes in both depths decreased, while Acidobacteria and Actinobacteria at both depths gradually increased (Figure 4A,B). Bacteroidetes, which prefer a nutrient-rich environment and mainly decompose simple organic compounds, are the r-strategists [11,13]. Furthermore, we observed that Bacteroidetes were positively correlated with the soil pH (Figure S2). Although our study showed more soil nutrients in the late stage of vegetation succession, a low soil pH might reduce the relative abundance of Bacteroidetes [5]. Acidobacteria and Actinobacteria, which participated in the decomposition of stubborn organic matter, tend to be the k-strategists [11]. Stubborn organic matter concentrations in litters improve with the vegetation succession, and the late succession stages are more conducive to Acidobacteria and Actinobacteria growth [4]. The results above demonstrate that, with the vegetation succession, the bacterial community trend changed from r-strategy to k-strategy [12]. In our study, it was interesting that the Proteobacteria, which tended to be the r-strategy groups, did not decrease significantly (Figure 4A,B), which could be due to the multitudinous subgroups of Proteobacteria and their adaptability [51,52]. We found that Ascomycota was the leading phyla in all four successional stages for the fungal communities (Figure 4C,D). At the 0–10 cm soil depth, Ascomycota was dominant in secondary forests, while Basidiomycetes were enriched in grassland (Figure 4C). This result was in line with the findings of Wang et al. [50] but contrary to some other results [2,12]. The variation of the SOC and TN contents could explain this phenomenon. The SOC and TN increased with the succession in this study (Table 1), with a positive correlation with Ascomycota and a negative correlation with Basidiomycetes, respectively (Figure S3). We also discovered that the major fungal phyla at the 10–20 cm depth were not significantly affected by the vegetation succession (Figure 4D), indicating that the succession of major fungal phyla at the 10–20 cm depth did not rely on soil nutrient dynamic changes [20]. In conclusion, considering the variations in the compositions of the soil bacterial and fungal communities, the bacteria and fungi at the two soil depths might follow different succession trajectories.

4.3. Changes in Ecological Function of Soil Microbial Communities during Vegetation Succession

There were significant differences in the ecological functions of the soil bacterial and fungal communities at all successional stages at both soil depths (Figure 5 and Figure 6), which was in agreement with some previous research [1,53]. Our study found that the soil bacterial function was diverse at both depths in the different successional stages. At the four succession stages of vegetation, the relative abundance of the functional genes of carbohydrate metabolism was the highest (Figure 5). This finding agreed with the results of Jiang et al. They also suggested that carbohydrate metabolism was the dominant function of bacteria, which was necessary for the growth of soil bacterial communities [54]. At both soil depths, nucleotide metabolism, related to cell homeostasis, was enriched in grassland, while energy metabolism, metabolisms of the cofactors and vitamins, and the translation and metabolism of terpenoids and polyketides were significantly increased with the succession (Figure 5). This was due to the changes in composition and diversity of the bacterial communities in the soil caused by vegetation succession affecting the soil bacterial ecological functions [54,55]. It has been previously documented that, with vegetation succession, the improvement in soil nutrients might increase the soil bacterial functional diversity [56]. For soil fungal functional groups, the fungal groups of pathotroph and saprotroph prefer to live in nutrient-rich environments, as fungal functional groups have habitat-specific adaptations [57]. In our research, pathotroph and saprotroph at both soil depths increased following the vegetation succession, while pathotroph–saprotroph dominated in shrubland (Figure 6), which agreed with some previous findings [4,57]. This result could be caused by two aspects. Firstly, vegetation succession changes the abundance and diversity of fungi and results in a corresponding change in the fungal functional diversity [51,57]. Secondly, some soil fungi are able to alter their trophic modes to adapt to the current living environment [58]. In addition, the unknown function of the fungi at both depths had the highest value in grassland, and their relative abundance was 51.98%~68.28% (Figure 6), which provides a momentous research direction for the further study of soil fungal ecological functions in karst areas.

4.4. Factors Affecting Soil Microbial Communities during Vegetation Succession

Vegetation succession directly affects soil microbial communities or indirectly affects them through the soil properties [59,60]. Based on the results of the RDA, the SOC was the crucial soil factor influencing the community change of the bacteria, yet it only had a noteworthy impact on the soil bacteria at the 0–10 cm (Figure 7A,B). The soil TN and TP were also important factors that affected the bacterial communities at both soil depths (Figure 7A,B). Jiang et al. obtained similar results and found that the SOC, TN, and TP in the soil had a significant association with the community of bacteria [2]. Moreover, the SOC, TN, and TP were positively related to Nitrospirae and Actinobacteria at two soil depths (p < 0.05) but negatively related to Chloroflexi and Verrucomicrobia in our study (p < 0.05) (Figure S2), reflecting that the responses of different bacterial communities to soil environmental factors are not consistent [56,61]. We noticed that NH4+-N mainly affected the bacteria in the topsoil, while NO3−-N mainly affected the bacteria in the subsoil (Figure 7A,B). Nitrogen has two forms of NH4+-N and NO3−-N. NO3−-N has high mobility in soil and is prone to leaching into the lower layers with water compared to NH4+-N. This may lead to different bacterial responses to the available nitrogen at different soil depths [62,63]. Yuan et al. revealed that the main soil factor influencing the bacterial community in the topsoil was NH4+-N [64]. Liu et al. believed that NO3−-N dramatically affected the subsoil bacterial community [65]. In our study, the SOC was the only soil factor that significantly influenced the soil fungal community (Figure 7C,D). At both soil depths, the SOC had a positive correlation with Ascomycota and Mortierellomycota (p < 0.05) and a negative association with Basidiomycota (p < 0.05) (Figure S3). Previous studies have also shown that the SOC is vital in affecting soil fungal survival [50,57]. Soil enzymes, an active component in soil ecosystems, affect the soil microbial diversity and composition [22]. In our research, the impact of soil enzymes on soil bacterial and fungal community changes was weak, but the effect on individual bacterial or fungal species was significant (Figure 7, Figures S2 and S3). There are many other environmental factors that influence changes in soil bacterial and fungal communities during vegetation succession, and the effects of other environments on soil bacterial and fungal communities need to be further investigated.

5. Conclusions

In this research, we manifested the response of soil bacterial and fungal communities and their functional characteristics at both soil depths with the succession of vegetation. Our study demonstrated that, as the vegetation succession progressed, the bacterial and fungal communities and their dominant phyla exhibited different succession patterns at both soil depths. Vegetation succession affected the soil microbial community structure and functional traits, in which soil fungi were mainly influenced by the succession stage, and soil bacteria were mainly influenced by soil property changes caused by the vegetation succession. In order to promote the restoration of karst ecosystems, it is necessary to further study the mechanisms of microbial ecological function and soil carbon and nitrogen cycling, so as to carry out targeted protection and management.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f14081562/s1. Figure S1: Principal coordinate analysis (PCoA) of soil bacterial (A,B) and fungal functions (C,D) in all successional stages at the 0–10 cm and 10–20 cm depths. Figure S2: Correlation analysis between bacterial-dominant phylum and soil properties at the 0–10 cm (A) and 10–20 cm (B) soil depths among the four succession stages in a karst region. Figure S3: Correlation analysis between fungal-dominant phylum and soil properties at the 0–10 cm (A) and 10–20 cm (B) soil depths among the four succession stages in a karst region. Table S1: Basic traits of different karst vegetation successional stage sample plots. Table S2: ANOSIM tests (Bray–Curtis distance) for the soil bacterial and fungal communities at the 0–10 cm and 10–20 cm depths within different stages of vegetation succession. Table S3: Pearson’s correlation analysis between the microbial alpha diversity and soil properties at the 0–10 cm and 10–20 cm depths.

Author Contributions

Conceptualization, Y.L. and Q.T.; methodology, Y.L. and Y.Y.; software, Y.L. and S.Z.; validation, Y.L., Q.T. and C.Y.; formal analysis, Y.L. and Q.T.; investigation, Q.T., P.W. and Y.C.; resources, Y.L., Q.T. and C.Y.; data curation, Y.L. and Q.T.; writing—original draft preparation, Y.L. and Q.T.; writing—review and editing, Y.L., F.D. and C.Y.; visualization, Y.L., Y.C. and Y.Y.; supervision, Y.L. and S.Z.; project administration, F.D. and P.W.; and funding acquisition, F.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the National Natural Science Foundation of China (No.32060244) and the Forestry Reform and Development Fund of Guizhou Province (No. (2022)36).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We would like to acknowledge Zhou Hua for correction and improvement of the English in the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 01562 g001 550
Figure 1. Study area and sample plots distribution. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively.
Figure 1. Study area and sample plots distribution. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively.
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Figure 2. Soil bacterial (A–D) and fungal (E–H) alpha diversities in different soil depths at each stage of the vegetation succession. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
Figure 2. Soil bacterial (A–D) and fungal (E–H) alpha diversities in different soil depths at each stage of the vegetation succession. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
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Figure 3. The principal coordinate analysis (PCoA) in the communities of soil bacteria (A,B) and fungi (C,D) among the four successional stages at both soil depths. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively.
Figure 3. The principal coordinate analysis (PCoA) in the communities of soil bacteria (A,B) and fungi (C,D) among the four successional stages at both soil depths. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively.
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Figure 4. Soil bacterial (A,B) and fungal (C,D) community compositions and relative abundance ratio (E,F) within the four vegetation succession stages at the two soil depths. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Prot: Proteobacteria; Acid: Acidobacteria; Acti: Actinobacteria; Chlo: Chloroflexi; Nitr: Nitrospirae; Verr: Verrucomicrobia; Bact: Bacteroidetes; Plan: Planctomycetes; Late: Latescibacteria; Tect: Tectomicrobia; Gemm: Gemmatimonadetes; Firm: Firmicutes; Asco: Ascomycota; Basi: Basidiomycota; Mort: Mortierellomycota; Roze: Rozellomycota. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
Figure 4. Soil bacterial (A,B) and fungal (C,D) community compositions and relative abundance ratio (E,F) within the four vegetation succession stages at the two soil depths. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Prot: Proteobacteria; Acid: Acidobacteria; Acti: Actinobacteria; Chlo: Chloroflexi; Nitr: Nitrospirae; Verr: Verrucomicrobia; Bact: Bacteroidetes; Plan: Planctomycetes; Late: Latescibacteria; Tect: Tectomicrobia; Gemm: Gemmatimonadetes; Firm: Firmicutes; Asco: Ascomycota; Basi: Basidiomycota; Mort: Mortierellomycota; Roze: Rozellomycota. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
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Figure 5. Variations of the soil bacterial function at both soil depths in the different successional stages. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
Figure 5. Variations of the soil bacterial function at both soil depths in the different successional stages. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
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Figure 6. Variations of the soil fungal function at both soil depths in the different successional stages. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
Figure 6. Variations of the soil fungal function at both soil depths in the different successional stages. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
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Figure 7. The redundancy analysis (RDA) of the soil properties and soil bacterial (A,B), and the fungal (C,D) community composition under different vegetation succession stages at both soil depths. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. SOC, soil organic carbon; TN, total nitrogen; TP, total phosphorus; AP, available phosphorus; NH4+-N, ammonia nitrogen; NO3−-N, nitrate nitrogen; Leu, leucine aminopeptidase; Ace, acetylglucosaminidase; Glu, glucosidase. Prot: Proteobacteria; Acid: Acidobacteria; Acti: Actinobacteria; Chlo: Chloroflexi; Nitr: Nitrospirae; Verr: Verrucomicrobia; Bact: Bacteroidetes; Plan: Planctomycetes; Late: Latescibacteria; Tect: Tectomicrobia; Gemm: Gemmatimonadetes; Firm: Firmicutes; Asco: Ascomycota; Basi: Basidiomycota; Mort: Mortierellomycota; Roze: Rozellomycota.
Figure 7. The redundancy analysis (RDA) of the soil properties and soil bacterial (A,B), and the fungal (C,D) community composition under different vegetation succession stages at both soil depths. GL, SL, SF, and PF represent grassland, shrubland, and secondary and primary forests, respectively. SOC, soil organic carbon; TN, total nitrogen; TP, total phosphorus; AP, available phosphorus; NH4+-N, ammonia nitrogen; NO3−-N, nitrate nitrogen; Leu, leucine aminopeptidase; Ace, acetylglucosaminidase; Glu, glucosidase. Prot: Proteobacteria; Acid: Acidobacteria; Acti: Actinobacteria; Chlo: Chloroflexi; Nitr: Nitrospirae; Verr: Verrucomicrobia; Bact: Bacteroidetes; Plan: Planctomycetes; Late: Latescibacteria; Tect: Tectomicrobia; Gemm: Gemmatimonadetes; Firm: Firmicutes; Asco: Ascomycota; Basi: Basidiomycota; Mort: Mortierellomycota; Roze: Rozellomycota.
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Table
Table 1. Variations of the soil properties among the four vegetation successional stages at both soil depths.
Table 1. Variations of the soil properties among the four vegetation successional stages at both soil depths.
Soil PropertiesDepth (cm)Successional Stages
GrasslandShrublandSecondary ForestPrimary Forest
pH0–107.11 ± 0.08 a7.07 ± 0.21 a6.95 ± 0.25 a6.84 ± 0.19 a
10–207.13 ± 0.07 a7.06 ± 0.23 a7.04 ± 0.09 a7.02 ± 0.14 a
SOC (g·kg−1)0–1033.37 ± 2.37 b60.4 ± 7.71 a58.82 ± 8.26 a77.19 ± 5.98 a
10–2027.98 ± 3.84 b44.38 ± 9.82 ab33.63 ± 5.36 b55.16 ± 6.17 a
TN (g·kg−1)0–103.41 ± 0.89 c6.35 ± 0.77 b6.60 ± 0.68 b8.82 ± 0.54 a
10–202.68 ± 0.59 b5.05 ± 1.13 a4.96 ± 0.58 a6.01 ± 0.35 a
TP (g·kg−1)0–100.49 ± 0.10 b1.12 ± 0.15 a0.84 ± 0.08 a0.95 ± 0.05 a
10–200.42 ± 0.09 b0.96 ± 0.17 a0.84 ± 0.08 a0.73 ± 0.10 ab
AP (mg·kg−1)0–107.08 ± 1.03 a6.79 ± 1.22 a5.53 ± 0.69 a7.05 ± 0.72 a
10–204.12 ± 0.77 a5.72 ± 1.27 a3.36 ± 0.62 a3.77 ± 0.49 a
NH4+-N (mg·kg−1)0–1013.69 ± 2.05 c22.03 ± 4.77 bc25.60 ± 3.34 b36.52 ± 4.17 a
10–208.98 ± 1.26 c15.12 ± 3.66 bc18.50 ± 1.99 b26.60 ± 2.33 a
NO3−-N (mg·kg−1)0–100.23 ± 0.11 b0.49 ± 0.11 ab1.35 ± 0.22 a1.37 ± 0.66 a
10–200.11 ± 0.06 b0.55 ± 0.33 ab1.48 ± 0.43 ab2.13 ± 1.00 a
Leu (μmol·h−1·g−1)0–10262.88 ± 54.62 b555.51 ± 98.54 a418.59 ± 46.35 ab305.93 ± 60.21 b
10–20146.17 ± 36.44 b644.16 ± 119.56 a354.75 ± 90.11 b173.13 ± 38.00 b
Ace (μmol·h−1·g−1)0–1018.21 ± 3.86 b74.07 ± 17.46 a35.16 ± 6.83 b26.25 ± 2.98 b
10–2019.90 ± 4.81 b64.59 ± 8.90 a25.25 ± 5.15 b24.63 ± 4.81 b
Glu (μmol·h−1·g−1)0–1045.27 ± 12.43 ab97.88 ± 28.54 a66.32 ± 16.01 ab34.72 ± 9.89 b
10–2031.83 ± 5.54 b114.91 ± 32.74 a34.69 ± 7.45 b27.97 ± 6.35 b
Note: SOC, soil organic carbon; TN, total nitrogen; TP, total phosphorus; AP, available phosphorus; NH4+-N, ammonia nitrogen; NO3−-N, nitrate nitrogen; Leu, leucine aminopeptidase; Ace, acetylglucosaminidase; Glu, glucosidase. Data are the means ± standard error (n = 3). Different letters indicate significant differences in the four vegetation types at the same soil depth (p < 0.05).
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Li, Y.; Tang, Q.; Yuan, C.; Zhu, S.; Ye, Y.; Wu, P.; Cui, Y.; Ding, F. Changes in Community Structure and Functional Characteristics of Soil Bacteria and Fungi along Karst Vegetation Succession. Forests 2023, 14, 1562. https://doi.org/10.3390/f14081562

AMA Style

Li Y, Tang Q, Yuan C, Zhu S, Ye Y, Wu P, Cui Y, Ding F. Changes in Community Structure and Functional Characteristics of Soil Bacteria and Fungi along Karst Vegetation Succession. Forests. 2023; 14(8):1562. https://doi.org/10.3390/f14081562

Chicago/Turabian Style

Li, Yuanyong, Qian Tang, Congjun Yuan, Sixi Zhu, Yuyan Ye, Peng Wu, Yingchun Cui, and Fangjun Ding. 2023. "Changes in Community Structure and Functional Characteristics of Soil Bacteria and Fungi along Karst Vegetation Succession" Forests 14, no. 8: 1562. https://doi.org/10.3390/f14081562

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