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Article

Response of the Soil Fungal Community and Its Function during the Conversion of Forestland to Tea Plantations: A Case Study in Southeast China

by
Feng Wang
1,2,3,
Yuzhen Chen
2,
Xiaomin Yu
3,
Wenquan Yu
2,*,
Zhiming You
2 and
Zhenbiao Yang
3
1
College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2
Tea Research Institute, Fujian Academy of Agricultural Sciences, No. 104 Pudang Road, Xindian Town, Jin’an District, Fuzhou 350012, China
3
FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(2), 209; https://doi.org/10.3390/f14020209
Submission received: 26 November 2022 / Revised: 14 January 2023 / Accepted: 18 January 2023 / Published: 21 January 2023
(This article belongs to the Special Issue Dynamics of Upland Soil for Agroforestry Crops)
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Abstract

:
Land-use change is one of the most important driving factors of change in soil microbial diversity. Deforestation for tea plantations has transformed large areas of forestland in hilly areas of Southeast China. However, its impact on the soil fungal community structures and functions is still understudied. We compared the soil fungal communities and their functions in forestland (FD), a 3-year-old tea plantation (ZC3) and a 30-year-old tea plantation (ZC30) at 0–20 cm and 20–40 cm soil depths. The soil fungal community compositions and potential functions were analyzed using high-throughput sequencing techniques coupled with FUNGuild analysis. The results showed that the initial conversion from forestland to tea plantations significantly decreased soil fungal diversity. With an increase in the tea plantation age, the soil fungal diversity rebounded. The dominant phyla included Ascomycota, Basidiomycota, unclassified_k_fungi and Mortierellomycota, which were identified in all soil samples and accounted for 90% of all fungal communities. Non-metric multidimensional scaling analysis (NMDS) indicated that the soil fungal community was more responsive to the duration of tea planting than to the soil depth. FUNGuild analysis showed that the relative abundance of pathogenic and pathotrophic-saprotrophic fungi was higher while saprotrophs were lower in ZC30 compared with FD. Among the analyzed soil properties, soil available nitrogen, available phosphorus, available potassium and bulk density were the prime factors affecting the abundance and diversity of soil fungal community compositions. Network analysis showed that fungal microbial taxa increased positive interactions to enhance the adaptability of fungal microorganisms to long-term tea planting. Collectively, our results provide a clear view on the dynamic yet differential responses of fungal communities to land-use changes, and further emphasizes the need for long-term conventional tea plantations to adopt sustainable agricultural practices to reduce soil pathogenic fungi.

1. Introduction

Soil is a kind of non-renewable resource, which is under great threat from intensive human activities such as agricultural production and graziery [1]. Soil microorganisms are usually considered to be the indispensable link between the soil and the vegetation ecosystem. As the most important participants in ecosystem functioning, soil fungi contribute significantly to soil matter cycling, soil aggregates formation, energy transmission and plant net primary production [2,3,4].
Land use change was considered to be an intensive human activity that poses the most serious threat to soil biodiversity and ecosystem function [5]. In the low hilly land of southeastern China, large natural forest areas have been converted to tea plantations due to economic incentives [6]. This transition can lead to a large disturbance in the ecosystem, resulting in vegetation diversity decline, soil carbon loss, land degradation and greenhouse gas emission [7]. All these changes are well known for their effects on soil fungal communities, and many studies have recorded the changes in soil fungal communities due to land-use changes (especially long-term cultivation and utilization) [7,8,9]. On the one hand, differences in the amount and chemical properties of vegetation litter, roots and sediments during forest clearing have led to changes in the soil fungal abundance [10]. On the other hand, the soil physiochemical properties (such as soil pH, moisture, nutrient content, texture and soil organic matter) have obviously varied due to frequent agronomic management practices, leading to varying effects on the soil fungal community structure [11,12].For example, the soil fungal diversity (species richness) decreased, the fungal community composition was substantially altered, and generalist fungi were strongly enriched when a tropical forest (primary and secondary forests) was converted to pasture in the Brazilian Amazon rainforest [13], whereas it simply influenced soil fungal composition in the semi-arid Loess Plateau of China [14]. Likewise, afforestation of cropland generally reduced soil fungal diversity (decreased by 23.76%–57.88%) and changed fungal functional groups (higher abundance of saprotrophs and ectomycorrhizal in Platycladus orientalis and Pinus tabuliformis), and this change was mainly due to the tree species [15]. Additionally, some studies have also shown that the composition (including classification and function) of soil fungal communities does not change much with land use, but the soil fungi function is affected by the legacy of land-use history [16,17]. Although many studies have confirmed the response of soil fungal communities to land-use changes, great uncertainty still exists due to differences in climatic conditions, soil types, cultivation duration and land-use history. Therefore, the evolution trend in soil fungal community structure and function depends on the aboveground vegetation and specific agricultural practices.
Tea is an important economic crop plant that is widely grown in tropical and subtropical regions throughout the world [18]. Tea plantations in China, which is the biggest tea producer, are usually developed from wasteland or forestland. More than 20 million tea farmers have planted more than 3.06 million hectares of tea plantations in China, and this figure has been continuously increasing [19].In general, the expansion of tea cultivation in some areas has displaced the natural vegetation such as forests, shrubs and grasslands. Such land-use intensification inevitably influences soil physicochemical and biological properties, which in turn, causes soil degradation and a dramatic yield decline following long-term tea planting [20,21]. Adverse effects associated with the conversion of forestland to tea plantations on soil physicochemical properties typically include decreased soil pH, accumulation of aluminum, fluorine and hydroxybenzene, loss of soil organic carbon, imbalance in the available soil nutrients and deterioration of the soil structure [19,22,23]. The diversity and functions of soil fungal communities in tea plantations are strongly influenced by a myriad of factors such as soil fertility, elevational gradients, tea cultivation intensity and duration, fertilization strategies, as well as ecological conditions [24,25,26,27].
Previous studies have largely concentrated on fungal diversity and community compositions in tea plantations, but ignored the effects of soil depth and tea plantation ages on fungal interactions and functional groups. In the hilly areas of Southeast China, tea plantations have continuously expanded, with extensive areas of forests being converted to tea plantations [28]. This provides an ideal test platform to investigate whether land use change affects the soil microbial diversity. In this study, high-throughput sequencing was used to study the short-term and long-term influences of forestland conversion to tea plantations on the soil fungal community compositions and functions in eastern Fujian province. The aims of this study were to investigate (1) how dominant soil fungal taxa respond to the conversion from forestland to tea plantations, and whether their compositions and responses are affected by the duration of tea planting; (2) whether land-use-related changes would be concentrated in the topsoil relative to the subsoil; (3) what role the soil physicochemical properties play in terms of the effect on the fungal community change.

2. Material and Methods

2.1. Site Selection and Soil Sampling

The study sites were located in Makeng Village (119°24′ E, 26°59′ N, approximately 650 m altitude), Zhouning County, Fujian Province, which is one of the main tea-producing regions in China [29]. The location has a subtropical monsoon climate with an annual illumination, rainfall and temperature of 1600 h, 1920 mm and 16.5 °C, respectively. Most of the tea plantations at the sites were transformed from forestland, and tea was planted in terraces. The soil type is classified as acidic red soil, developed from weathered granite material. The land-use type was considered as a typical hilly tea plantation. Soil from the adjacent forestland was sampled for comparison and is referred to as “FD” hereafter. The distance between forestland and the tea plantations was no more than 50 m. Soil samples from tea plantations with two different plantation ages (3 and 30 years old) were collected in our study and referred to as “ZC3” and “ZC30”. The environmental conditions (such as slope direction, slope position and elevation) and agronomic measures were similar in these tea plantations. The tea plantations were managed according to conventional farming with fertilizer amounts of 2250 kg.hm−2 (m (N):m (P2O5):m (K2O) = 15:15:15). Fertilizers were applied to the tea plantation soil three times, in spring (end of February to early March), autumn (late August) and winter (end of December to January), with an application proportion of 3:3:4, and the top dressing and base fertilizers were located at the same position.
Sampling squares were set up within 20 m along the slope in the same slope direction, and three 15 m × 15 m sampling squares were set up. In tea plantations, five core samples (5 cm in diameter) were collected in 5 different tea rows. In forestland, five samples were collected along a S-shaped pattern. The five samples were mixed into a composite sample. Each plot was sampled for soil layers 0–20 cm and 20–40 cm, 6 soil samples were collected from each plot on 5 December 2016. Each soil sample was further divided into two portions: one portion was rapidly stored at −80 °C for soil DNA extraction and molecular analysis. The other portion was air-dried for the measurement of soil organic matter (SOM), available N (AN), available P (AP), available K (AK), pH, available Fe (AFe), exchangeable calcium (ACa) and bulk density (BK).

2.2. Soil Physical and Chemical Analyses

SOM was measured using the dichromate oxidation method (K2Cr2O7-H2SO4). AN was determined by the alkaline hydrolysable method. AP was extracted by hydrochloric acid and ammonium fluoride and determined using the molybdenum blue method [30]. AK was extracted by ammonium acetate and determined by flame photometry [21]. Soil pH was measured using a pH meter in suspensions (1:2.5 soil/water). AFe was extracted by diethyl triamine pentaacetic acid (DTPA) and determined using atomic absorption spectrometry. ACa was extracted by ammonium acetate and determined using atomic absorption spectrometry. BK was measured using the ring knife method, and the soil samples were collected by the 100 cm3 ring knife [31]. The soil properties of the test plots are shown in Table S1.

2.3. Soil DNA Extraction, MiSeq Sequencing, Data Processing and Analysis

The DNA was extracted from a 500 mg fresh soil with a Soil E.Z.N.A.® Soil DNA Kit (Omega Bio-tek, Norcross, GA, USA) according to the manufacturer’s protocols. DNA quality and quantity were measured using Thermo Scientific’s NanoDrop 2000 (Thermo Scientific, Waltham, MA, USA). Amplification of the ITS1 region was performed with ITS1F and ITS2R primers [32]. The PCR conditions and primer sequences are listed in Table S2. The PCR products were sent to Majorbio Bio-Pharm Technology Co., Ltd. (Shanghai, China), and sequencing was performed on the Illumina MiSeq platform (PE250, Illumina, San Diego, CA, USA). An accession number PRJNA751692 has been assigned to the raw amplicon sequences deposited in the Sequence Read Archive (SRA).
The data obtained by Illumina sequencing were analyzed using the QIIME (v.1.9.1, http://qiime.org/install/index.html) software package [33]. Sequences with lengths less than 150 bp or with mononucleotide repeats were eliminated. FLASH was used to assemble the filtered pair-end reads. The resulting high-quality sequences were clustered into operational taxonomic units (OTUs) using the Uparse (v. 7.0.1090, http://drive5.com/uparse/) at a 97% sequence similarity [34]. Finally, a representative sequence for OTUs was assigned to sequences deposited in the UNITE database for fungi (v.8.0, http://unite.ut.ee/index.php) [35].

2.4. Statistical Analysis

In this study, we used Shannon, Simpson, Chao1, Sobs and ACE indices to indicate the alpha diversity. Non-metric multidimensional scaling (NMDS) was used to explore the differences in fungal communities based on Bray-Curtis distances. Redundancy analysis (RDA) was carried out to determine the effects of soil environmental factors on the fungal community composition. Before RDA analysis, soil environmental factors were screened to retain less multicollinearity environmental factors by variance inflation (VIFs) analysis, until the selected environmental factors corresponding VIF values were all less than 10. Meanwhile, the effects of land use and soil depth on the fungal community were detected by using permutational multivariate analysis of variance (PERMANOVA) [36]. The NMDS, PERMANOVA and RDA were both carried out by the vegan package of R project (v.3.3.1) [37]. Linear discriminant analysis (LDA) effect size (LEfSe) was carried out to find the fungal biomarkers of forestland and tea plantations, and the LDA score was set to 3.5 [38]. Network analysis was constructed to investigate the co-occurrence patterns of fungal taxa between forestland and tea plantations using the NetworkX package in the Python environment. To simplify the network for better visualization, we only examined those results with a strong Spearman’s coefficient (R > 0.80, p < 0.05) of the top 100 OTUs. The visualization of co-occurrence was constructed by Gephi software (v 0.90.7, https://gephi.org/). Furthermore, fungal guilds were predicted using the FUNGuild (v1.0, http://www.funguild.org/) [39]. Functional groups were assigned to a guild with confidence levels of “highly probable” “probable” and “possible”; we retained the comparison results with “highly probable” and “probable”. The OTUs were matched with functional guilds in approximately 60% of cases. All of the data for the soil fungi were analyzed using the free online Majorbio Cloud Platform (www.majorbio.com, accessed on 17 February 2022).
Pearson correlations between dominant fungal abundance, alpha diversity and soil properties were calculated at the 0.05 probability level in SPSS software (v.19.0, SPSS Inc., Chicago, IL, USA). Different soil OTUs, dominant phyla, and genera were compared with one-way ANOVA. Two-way ANOVA was performed using different soil depths and sample land use as the main effects.

3. Results

3.1. Effects of Forestland Conversion to Tea Plantations on Soil Fungal Communities

Based on fungal OTUs, Venn diagrams were generated to study the differences in fungal communities in soil samples. In total, 6079 fungal OTUs were detected, of which 1541, 869, 958, 1226, 790 and 695 were detected only in samples from FDA, ZC3A, ZC30A, FDB, ZC3B and ZC30B, respectively, and 106 core fungal OTUs were shared by all samples (Figure 1). Specifically, the numbers of OTUs in the FD samples were higher than those in the ZC3 samples.
Fungal OTUs across 18 samples were assigned to 13 different phyla, 50 classes, 123 orders, 266 families and 485 genera. The dominant phyla included Ascomycota (43.46%), Basidiomycota (27.76%), unclassified_k_fungi (12.36%) and Mortierellomycota (7.91%), accounting for 90% of all fungal communities (Figure 2a). One-way ANOVA showed that the relative abundance of Basidiomycota, Glomeromycota, Chytridiomycota and Mucoromycota showed significant differences among samples at the 0–20 cm soil depth (Figure 3a). At the 20–40 cm soil depth, the relative abundance of Ascomycota, Basidiomycota and unclassified_k_fungi showed significant differences among different soil samples (Figure 3b). At the genus level, Saitozyma (15.13%), an unclassified genus of fungi (12.50%), an unclassified genus of Archaeorhizomycetes (8.44%), Mortierella (7.80%) and an unclassified genus of Agaricales (7.20%) were the most dominant genera (Figure 2b). The relative abundance of two unclassified genera from Basidiomycota and Agaricales significantly decreased when forestland was converted to tea plantations, whereas the relative abundance of Fusarium, Pseudopestalotiop, and two unclassified genus from Arcaeorhizomycetes and Glomeromycota significantly increased at the 0–20 cm soil depth (Figure 3c).
In this study, we used LEfSe analysis to distinguish microbial groups based on planting systems and soil depths. In general, the fungal taxa were impacted more by land use. At the 0–20 cm soil depth, the LDA scores for 60 taxa were greater than 3.5 in fungal groups, including 17 taxa in FDA, 21 in ZC3A and 22 in ZC30A (Figure S1a). Additionally, 38 taxa exhibited significant differences at the 20–40 cm soil depth, with 12 taxa in FDB, 10 in ZC3B and 16 in ZC30B (Figure S1b). Overall, the 30-year-old tea plantation soil had slightly more fungal biomarkers than the other two planting systems at all sampled soil depths.

3.2. Effects of Forestland Conversion to Tea Plantations on Soil Fungal Alpha and Beta Diversities

Two-way ANOVA showed that fungal alpha diversity is extremely significantly by land use and soil depths on Sobs, ACE and Chao1 diversity indices (p < 0.01, Table 1), with FD showing a significantly higher diversity than ZC3 and ZC30 at the two soil depths (Table 1). No significant effect was observed for land-use types, depths and their interactions on the Simpson index. In general, after forestland was converted to tea plantations, soil fungal alpha diversity decreased significantly at the beginning of cultivation, and then increased with the increase in the age of the tea plantation.
NMDS was used to analyze and visualize the structure of the fungal community (Figure 4). NMDS analysis showed that the fungal community structures showed no significant changes between the two soil depths (Figure 4a, R = 0.0844, p = 0.104). The permutational multivariate analysis of variance result also verified this difference (R2 = 0.038, p = 0.538). The substantial changes in the soil fungal community structure were noted between the processes of forestland conversion to tea plantations (FD vs. ZC3, R2 = 0.60, p = 0.003; FD vs. ZC30, R2 = 0.59, p = 0.004; ZC3 vs. ZC30, R2 = 0.28, p = 0.016) (Figure 4b; Table 2).

3.3. Fungal Co-Occurrence Networks and Their Topological Features

In this study, we used OTUs to construct a co-occurrence network to analyze interactions between fungal taxa. Multiple network topology measurement consistently showed that the fungal networks exhibited significant differences in the three groups (Figure 5 and Table 3). There were more complex and stable co-occurrence networks in tea plantations than in forestlands. Compared with FD, the number of edges were higher in CK3 and CK30 (from 695 to 845/873) (Table 3). The numbers of total edges, positive edges, average degree, average clustering coefficient, modularity and network density in the fungal networks typically increased as the tea plantation ages, while the average path length exhibited the opposite trend. Remarkably, the ratio of positive edges accounted for approximately 56.4% in FD, approximately 60.24% in ZC3, and approximately 62.77% in ZC30. Keystone species in fungal networks were also altered by tea planting (Figure 5 and Table S3). Most keystone species in FD and ZC3 belonged to the phylum Ascomycota (9 OTUs and 6 OTUs), but the keystone species in ZC30 was mainly from the unclassified_k__Fungi (OUT1398, OTU1355, OTU1232 and OTU1352) and Mortierellomycota (OTU2063 and OTU1580).

3.4. Effects of Forestland Conversion to Tea Plantations on Soil Functional Fungal Groups

Forestland conversion to tea plantations significantly changed the functional fungal groups in the soil. Seven main trophic modes were detected by FUNGuild. Based on the trophic mode, forestland and tea plantations were dominated by saprotrophs and symbiotrophs with a relative abundance ranging from 43.19% to 79.25% and from 2.02% to 32.82% in forestland and tea plantations, respectively. The two-way ANOVA indicated that the land use (L) significantly affected the symbiotrophs and saprotrophs-symbiotrophs (p < 0.01, Table S4), and soil depths (D) significantly affected the pathotrophs and saprotrophs-symbiotrophs, whereas the interaction between these variables had little influence (except for saprotrophs and saprotrophs-symbiotrophs). Among these, the proportion of pathogenic and pathotrophic-symbiotrophic fungi in ZC30A (18.37% and 29.74%) was significantly higher than in FDA and ZC3A (Table S2). The proportion of symbiotrophs in ZC3A (36.09%) was significantly higher than those identified in FDA and ZC30A (11.86% and 2.13%, respectively). Additionally, a significantly higher proportion of symbiotrophs were identified in the FDA (74.59%) in comparison to ZC3A (50.11%) and ZC30A (43.19%). At the 20–40 cm soil depth, the proportion of symbiotrophs in the ZC3B was significantly higher than those identified in FDB and ZC30B, and the proportion of saprotrophs-symbiotrophs in the FDB was significantly higher than in ZC3B and ZC30B.
We found 79 guilds from the FUNGuild database when predicting the fungal functional potentials. The relative abundance of functional fungal guilds, such as animal pathogen, endophyte-litter saprotroph-soil saprotroph-undefined saprotroph, endophyte-litter saprotroph-wood saprotroph, fungal parasite, fungal parasite-plant pathogenic fungi-plant saprotroph and plant pathogen remained unaffected across groups (Table S5). In addition, there were interaction effects of L × D on animal pathogen-plant pathogen-undefined saprotroph, bryophyte parasite-ectomycorrhizal-ericoid mycorrhizal-undefined saprotroph-wood saprotroph, endophyte-litter saprotroph-soil saprotroph-undefined saprotroph, endophyte-soil saprotroph, soil saprotroph and undefined saprotroph (Table S5). At the 0–20 cm soil depth, the relative abundance of fungal parasites-undefined saprotrophs (25.56%) and soil saprotrophs (8.03%) in FDA were significantly higher than in ZC3A (9.86% and 0.73%) and ZC30A (17.11% and 0.15%). Additionally, a significantly higher proportion of animal pathogens-endophytes-lichen parasites-plant pathogens-soil saprotrophs-wood saprotrophs (9.16%), animal pathogen-plant pathogen-undefined saprotroph (1.03%) and fungal parasite-plant pathogen-plant saprotroph (8.84%) were identified in ZC30 in comparison to ZC3A (0.23%, 0.004% and 0.024%) and FDA (0.028%, 0.0024% and 0.015%) (Figure 6). A significantly higher percentage of arbuscular mycorrhizal, bryophyte parasite-ectomycorrhizal-ericoid mycorrhizal-undefined saprotroph-wood saprotroph, endophyte-litter saprotroph-wood saprotroph were found in ZC3A relative to FDA and ZC30A (Figure 6). At the 20–40 cm soil depth, the proportion of symbiotrophs in ZC3B was significantly higher than those identified in FDB and ZC30B, and the proportion of saprotrophs-symbiotrophs in FDB was significantly higher than in ZC3B and ZC30B.
The letters in different colors indicated significant differences in land use patterns (p < 0.05).

3.5. Relationship between Fungal Community Structure and Soil Properties

For fungal communities, AN and AP contents were positively correlated with Sobs, Shannon, ACE and Chao1 indices, and negatively correlated with the Simpson index (Table S6, p < 0.01). AFe showed positive correlations with Sobs, Shannon and ACE, and ACa showed positive correlations with ACE. BK showed negative correlations with Sobs, Shannon, ACE and Chao1 indices, and a positive correlation with the Simpson index. SOM and pH were not significantly correlated with fungal alpha diversity.
In all samples, Pearson correlation analysis showed that the fungal communities were significantly correlated with soil characteristics (Figure S2). Our RDA explained 40.33% and 35.04% of the variation in the fungal community at the phylum and genus levels (Figure 7). At the phylum level, RDA analysis showed that AN (R2 = 0.48, p = 0.01), AK (R2 = 0.42, p = 0.012) and ACa (R2 = 0.37, p = 0.042) had a clear impact on fungal community (Figure 6a and Table S7). Moreover, RDA results indicated that AN (R2 = 0.58, p = 0.001), AP (R2 = 0.37, p = 0.045) and BK (R2 = 0.48, p = 0.012) had an obvious influence on soil fungal community (Table S7).

4. Discussion

4.1. Forestland Conversion to Tea Plantations Decreases Soil Fungal Diversity

Fungi play an important role in soil energy flow and nutrient transformation, and their abundance and diversity reflect the efficiency of biological transformation, soil fertility and the ecological buffer capacity [40]. However, the process of fungal community formation in terrestrial soils is complex and depends on vegetation types, land use, farming practices and climatic conditions [14,41], and the results will be different because of the different sampling locations and sampling time [42]. In this study, using high-throughput sequencing and FUNGuild, we provided a clear point of the response and functions of the soil fungal community after forestland conversion to tea plantations in a mountainous region in Southeast China.
According to previous studies, plant composition and litter quality have strong impacts on soil fungal activity through several primary processes, including the production of litters, exuding from roots and directly interacting with root-associated or symbiotic fungi, as well as an indirect impact on fungal nutrient limitation by affecting fungal composition and soil nutrient supply [43,44]. In our study, the conversion of forestland into tea plantations had significant effects on soil fungal diversity at two soil depths (Table 1). Our results showed that the conversion of forestland to a 3-year-old tea plantation decreased soil fungal alpha diversities, which is consistent with previous studies showing that conventional tea planting could decrease the soil microbial diversity [6]. This finding may be due to the changes in soil properties caused by human agriculture (reclamation and continuous cultivation), which alter fungal diversity [45]. Four potential mechanisms could be involved. First, the original vegetation with high species diversity is replaced by a relatively single primary Camellia sinensis and the undergrowth species diversity potentially decreases with a significant loss in species richness [46]. In the meantime, the quantity and quality of litters undergo fundamental changes during tea planting. This was one of the possible reasons that led to a marked drop in soil fungal alpha diversities after tea planting in Mediterranean soils [47]. A meta-analysis based on 119 global forest degradation experiments worldwide revealed that forest degradation decreased soil fungal abundance and fungi-to-bacteria ratio across all anthropogenic land-use changes, and the soil microbial community compositions changed from K-strategist dominated to r-strategist dominated [48]. Second, close tea bushes grow in compact plantings relative to each other and toxic and antimicrobial substances in root exudates might accumulate in the Tieguanyin rhizosphere [20], which may have an obvious inhibiting effect on the soil microbial community. Third, during the conversion from forestland to tea plantations, frequent tillage (land clearance and plowing) destroys soil aggregates and consequently results in losses of soil organic matter at different soil depths [49], thereby decreasing the soil fungal alpha diversity in tea plantations. Finally, herbicides and pesticides used in tea plantations also have a negative effect on soil microbes [50]. In short, long-term monoculture cropping systems, the specific rhizosphere environment (acid and aluminum accumulation, Table S1 in Supplementary Materials) and accumulation of toxic and antibacterial substances all contribute to the decrease in the fungal community diversity in tea plantation soils.
Moreover, some studies have shown that tea plantation age has a significant effect on the microbial alpha diversity [20,21,51]. In our study, the soil fungal alpha diversity gradually increased with the age of tea plantation. Two potential mechanisms could be used to explain the promotion of soil fungal populations in tea plantations. First, the accumulation of SOM AN, AP and AFe in 30-year-old tea plantations was caused by litter and pruning persistently returning to the tea plantation (Table S1). Second, long-term fertilization increases soil nutrient contents in the tea plantation and soil microbial biomass and hence, soil samples from mature tea plantations occupy more OTUs and show a higher diversity than those of young tea plantations. Our result is similar to the result from Zhao et al. showing that the soil microbial diversity indices were apparently higher in a 25-year-old tea plantation compared with a 7-year-old tea plantation [51].

4.2. Forestland Conversion to Tea Plantations Shifts Soil Fungal Community Compositions

In the current study, the dominant phyla of the soil fungal community did not change during tea planting, but their relative abundance changed significantly (Figure 2). This study found that Basidiomycota and Ascomycota dominated the fungal community composition. As has been previously reported in soil fungal studies, these two groups were also the dominant fungal phyla in Longjing [52] and Oolong tea plantations [53]. In surveyed tea plantations, Ascomycota abundance increased, while Basidiomycota abundance decreased compared with forestland soil in the topsoil. The results of this study are consistent with previous studies that showed that Basidiomycota decreased and Ascomycota increased after tropical rain forest reclamation and conversion to rubber or palm plantations [16]. Other studies have also shown that a change in land use from forestland to a cultivated system (such as a plantation, economic forest, farmland and pasture) reduces the abundance of Basidiomycota [45]. Furthermore, we found that the relative abundance of Fusarium, Melanconiella, Pestalotiopsis, and Pseudopestalotiopsis in the Ascomycota phylum. increased significantly with continuous monoculture of tea plants. The Pestalotiopsis and Pseudopestalotiopsis are the main pathogens causing tea grey blight and red leaf spot [54]. In this study, the genus of Pestalotiopsis and Pseudopestalotiopsis were enriched in the ZC30 soils, and this could increase the risk of plant disease outbreaks, resulting in the loss of tea production [55]. Apparently, long-term tea planting creates new habitats that are colonized by fungal communities divergent from those in the forestland soil.
In the current study, the NMDS analysis revealed that long-term tea planting affects soil fungal communities (Figure 4). An earlier study found that long-term monoculture in a Tieguanyin tea plantation significantly affected the soil fungal communities [21]. This phenomenon has also been recorded in banana [56] and coffee cropping systems [57]. Moreover, we found no significant differences between the topsoil and subsoil fungal communities. Consistent with this assumption, soil depth and the bacterial community were more strongly correlated with each other than with the fungal community in the Loess Plateau [58] and a fallow field [59]. Conversely, most fungi grow as hyphae, which can grow up to a few centimeters in length. In addition, fungi also make spores, an efficient propagation stage that can spread through water or air, thus endowing them greater geographical mobility than bacteria.

4.3. Effects of Forestland Conversion to Tea Plantations on Fungal Co-Occurrence Networks and Functional Fungal Groups

Soil microbial communities do not develop and flourish in isolation, but instead form complex networks of associations to cope with a wide range of environmental stresses [60]. Hence, understanding the complex soil fungal network is crucial to predicting the response of soil fungi to environmental stresses. In general, the microbial communities with a complex network have a higher potential for resource and information transmission than the simpler networks. Thus, the complex microbial networks are considered to be more resistance to environmental pressures than simpler ones [61]. The network complexity of fungi has been found to reduce with land-use change from forest to rubber plantation in southwest China [2].Compared with natural forests, plantations significantly reduced the network complexity of the fungal community in a forest on eastern Hokkaido [62]. In tropical rainforests, the conversion of tropical rainforest to rubber plantations reduced soil fungal β diversity and network complexity, which resulted in a net loss of landscape-level diversity [63]. In this study, more nodes, edges, average connectivity, average clustering coefficient and network density were observed in the tea plantation networks than in the forestland networks. It can be concluded that relatively larger and more complex networks of fungal communities were found in the tea plantation than in the forestland, which is inconsistent with previous studies showing that tea planting could decrease the soil microbial network complexity. This is probably related to the tea variety and cultivating conditions [64]. There is a possibility that the soil fungal network is constantly disturbed by agricultural cultivation management practices, such as tillage, pesticides, fertilization, and weeding in tea plantations compared with forestland [6,65]. Due to measures of land consolidation for newly-cultivated tea plantations, the SOM, AN, AP, AK and AFe decreased in the 3-year-old tea plantation (Table S1). Soil nutrient resource limitations in ZC3 increased network complexity and further enhanced the fungal community stability [60]. Meanwhile, compared with FD and ZC3, the above positive relationships were enhanced in the ZC30 soils (by 6.37% and 2.53%, respectively), indicating that long-term tea plantations may have experienced higher nutrient competition among taxa. As some previous studies have shown, fertilizer inputs lead to changes in nutrients and carbons that create new niches [66].The use of mineral and organic fertilizers in older tea plantations provides ample amounts of readily available nutrients or easily decomposable substrates, which may increase the connectivity and interactions of fungal network [67]. In addition, keystone species in fungal networks were also altered by tea planting (Table S3), keystone species in fungal were derived from more phyla in FD. Overall, we presumed that the long-term fertilization might be a key factor in determining the complexity of the fungal network.
Supporting our hypothesis, the soil fungal guilds obviously differed among forestland and tea plantations at two soil depths, and saprotroph (60.49%) and symbiotroph-dominated (16.78%) communities were favored in forestland and tea plantations (Table S4), respectively. Compared with forestland, tea planting decreased the relative abundance of saprotrophs (e.g., soil saprotrophs and undefined saprotrophic fungi), whereas they increased the relative abundance of pathogenic and pathotrophic–saprotrophic fungi (e.g., plant–pathogen, animal pathogen–endophyte–lichen parasite–plant pathogen–soil saprotroph–wood saprotroph). Generally, saprotrophic fungi are very helpful in terms of soil nutrient utilization and organic matter decomposition [39], and symbiotrophic fungi are very useful for healthy growth, nutrient uptake and quality formation in most crops [68]. The potential fungal pathogens are thought to cause disease or have a negative effect on plant growth by attacking host cells for nutrients [69]. In this study, the percentage of symbiotrophic fungi in ZC3 was higher than that in ZC30 soil, whereas the abundance of pathogenic fungi in ZC30 soil was higher than that in forestland and ZC3, showing that long-term tea monoculture likely suffers a higher risk of soil-borne (or plant-borne) fungal diseases with the extension of continuous tea plantation years. Similarly, Marín et al. reported that conversion of high-altitude temperate forests to agricultural land in Chile increased the abundance of fungal pathotrophs, especially animal pathogens [70]. This observation might be due to the large amount of AP (112.00 mg.kg−1) in our study, and the potential roles of these symbiotic nutrients in plant nutrition, pathogen protection, stress tolerance and soil structure allocation may be counterbalanced by high soil phosphorus levels [71]. A recent study showed that high soil available phosphorus could exhaust plant beneficial microorganisms and increase the abundance of pathogenic bacteria, thus endangering plant health [72]. This study found that soil available phosphorus had a significantly positive correlation with pathogens, pathotrophs–saprotrophs, pathotrophs–saprotrophs–symbiotrophs and pathotrophs–symbiotrophs (Table S8). Therefore, tea gardens with high phosphorus content could reduce pathogenic microorganisms by reducing or not applying phosphorus to the soil in the short term, which is conducive to the coordinated development of soil microbial flora in tea gardens.

4.4. Effects of Soil Properties on Soil Fungal Community Compositions

During the conversion from forestland to tea plantations, the litter input, root expansion, root deposition, root exudates, fertilization and tillage directly affected the input and turnover of soil nutrients, and correspondingly affected the soil microenvironment [6,53] After forestland was converted to tea plantations, the soil pH and carbon were dramatically reduced (Table S1), and long-term tea planting generally increases available nutrients (especially available phosphorus). In this study, long-term continuous tea cropping resulted in the expected low pH (ZC30 soil pH value was 3.77~3.79) and a high effective phosphorus concentration, which was consistent with previous experimental results [6,23]. The increase in AN and AP from the ZC30 soil may be related to the long-term application of chemical fertilizer.
Soil properties such as available nutrients, pH, bulk density and hydrothermal conditions are important drivers of microbial community structure [73,74]. In this study, we found that the fungal community had a higher correlation with soil properties (Table S6, Figure S2). Hence, long-term tea planting have a significant impact on fungal community structure Soil carbon and nitrogen are key resources supporting most terrestrial microbial communities [75] and their turnover is closely related to soil fungi. Our findings suggest that the relative abundance of Basidiomycota was significantly and positively correlated with SOM and AN, whereas Mortierellomycota, Glomeromycota and Calcarisporiellomycota showed the opposite pattern. RDA showed that AN also significantly impacted fungal communities during long-term tea planting. These results support previous observations regarding the role of AN on the fungal community structure [76]. Similarly, most fungal abundant phyla were significantly and negatively correlated with BK, in agreement with the results by Zhao et al. [77]. Soil pH is one of the most important environmental factors influencing soil microbial communities. It was found that soil pH had a weak correlation with fungi [78,79]. However, a relatively narrow soil pH range (varying from 3.77 to 4.47) may have been insufficient to cause differences in the fungal communities, and the correlation patterns could vary in different soils. In addition, the AP content had a significant effect on the abundance of dominant fungal phyla and alpha diversity (Table S6; Figure S2), which were also demonstrated in previous studies in Pinus tabulaeformis [80] and forest reserves [81]. Additionally, microbial changes during long-term tea cultivation may not be exclusively attributed to soil properties changes, but also to long-term effects of tea plant residues or root exudates, which need to be further studied.

5. Conclusions

Taken together, the response and functions of soil fungal communities in the conversion of forestland to tea plantations was studied by Illumina high-throughput sequencing and FUNGuild. Long-term continuous tea monoculture changes the compositions and functional groups of soil fungal communities. The soil fungal diversity decreases significantly by tea planting (especially in the early stage of the tea plantation development), but the soil fungal network complexity shows the opposite trend. In addition, we also observe that tea planting enhances interactions between fungal microbial communities, suggesting that interspecific association could enhance the adaptation of fungal communities to the change of land use patterns. Furthermore, the long-term tea monoculture increases the relative abundance of pathogenic and pathotrophic–saprotrophic fungi, while decreases the relative abundance of beneficial fungi (saprotrophs). AN, AP, AK and BK may be the main factors affecting tea soil fungal diversity, community compositions and functional guilds. These results provide valuable information for understanding the long-term continuous monoculture problems of tea plants. In the future research, we will continue to examine how reduced chemical fertilizer application (especially phosphate) and sustainable tillage practices affect soil microbial community structure and function in tea plantations.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/f14020209/s1. Table S1: Effects of forestland conversion to tea plantations on soil physical and chemical properties; Table S2: Primer sets and thermal profiles used in PCR amplification; Table S3: Key species in soil fungal network under different land use; Table S4: Effects of forestland conversion to tea plantations on soil fungal trophic modes; Table S5: Effects of forestland conversion to tea plantations on soil fungal functional groups (guilds); Table S6: Pearson correlations between soil properties and fungal alpha diversity; Table S7: Correlations between soil fungal community and soil properties; Table S8: Pearson correlations between soil properties and fungal trophic modes; Figure S1: LEfSe indicating differences in the fungal taxa among forestland and tea plantation samples; Figure S2: Pearson correlations between soil properties and abundant fungal phyla (a) or fungal genera (b).

Author Contributions

Methodology, Z.Y. (Zhenbiao Yang); software, F.W. and Z.Y. (Zhiming You); validation, Y.C. and W.Y.; investigation, F.W., Y.C., Z.Y. (Zhiming You) and X.Y.; data curation, F.W. and W.Y. and X.Y.; writing—original draft, F.W.; writing—review and editing, F.W., W.Y. and X.Y.; project administration, W.Y.; funding acquisition, W.Y. and Z.Y. (Zhiming You). All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Fujian Funding Scientific Research Program (2020R1029001 and 2021R1029002), the National Science Foundation of Fujian Province (2021J01489), the Chinese Ministry of Science and Technology’s Special Program for Science and Technology Development in Fujian Province (2020L3030) and the Fujian Academy of Agricultural Sciences Science and Technology Innovation Team Program (CXTD2021006-1).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in the article and the supplementary materials.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Operational taxonomic unit (OTU)-based Venn diagram for soil fungi. FD: forestland; ZC3: 3-year-old tea plantation; ZC30: 30-year-old tea plantation. A and B indicate soil depths of 0–20 cm and 20–40 cm, respectively. The values on the histogram represent the number of OTUs.
Figure 1. Operational taxonomic unit (OTU)-based Venn diagram for soil fungi. FD: forestland; ZC3: 3-year-old tea plantation; ZC30: 30-year-old tea plantation. A and B indicate soil depths of 0–20 cm and 20–40 cm, respectively. The values on the histogram represent the number of OTUs.
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Figure 2. Phylum (a) and genus (b) levels of soil fungal abundance in different samples.
Figure 2. Phylum (a) and genus (b) levels of soil fungal abundance in different samples.
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Figure 3. Three comparison groups based on phylum and genus levels with FD, ZC3 and ZC30. (a–d) represent the significant tests at phylum and genus levels. *** p < 0.001; ** p < 0.01; * p < 0.05; NA p > 0.05.
Figure 3. Three comparison groups based on phylum and genus levels with FD, ZC3 and ZC30. (a–d) represent the significant tests at phylum and genus levels. *** p < 0.001; ** p < 0.01; * p < 0.05; NA p > 0.05.
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Figure 4. NMDS analysis evaluating differences in the fungal community structures according to Bray−Curtis distance. (a) NMDS results of the difference between the two soil depths. (b) NMDS results of overall community.
Figure 4. NMDS analysis evaluating differences in the fungal community structures according to Bray−Curtis distance. (a) NMDS results of the difference between the two soil depths. (b) NMDS results of overall community.
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Figure 5. Network and node classification of soil fungal genera among forestland and tea plantation samples. The network with modules colored by modularized classes has strong correlations (Spearman p > 0.80) and significant correlations (p < 0.05). The line between each pair of nodes represents strong positive (red) or negative (green) interactions. Nodes in a network are colored according to their OTUs, and the size of each node reflects its degree. Samples from two soil depths were mixed into one sample for network analysis. (a–c) stand for FD, ZC3, and ZC30, respectively.
Figure 5. Network and node classification of soil fungal genera among forestland and tea plantation samples. The network with modules colored by modularized classes has strong correlations (Spearman p > 0.80) and significant correlations (p < 0.05). The line between each pair of nodes represents strong positive (red) or negative (green) interactions. Nodes in a network are colored according to their OTUs, and the size of each node reflects its degree. Samples from two soil depths were mixed into one sample for network analysis. (a–c) stand for FD, ZC3, and ZC30, respectively.
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Figure 6. The relative abundance of putative fungal functional guilds under land use (L) and depths (D) based on the FUNGuild database. (a–f) stand for pathotroph, saprotroph, symbiotroph, pathotroph-symbiotroph, saprotroph-symbiotroph and pathotroph-saprotroph-symbiotroph, respectively.
Figure 6. The relative abundance of putative fungal functional guilds under land use (L) and depths (D) based on the FUNGuild database. (a–f) stand for pathotroph, saprotroph, symbiotroph, pathotroph-symbiotroph, saprotroph-symbiotroph and pathotroph-saprotroph-symbiotroph, respectively.
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Figure 7. Redundancy analysis of soil fungal community structure on soil characteristics (AN, AP, AK, pH, ACa and BK) in different samples. (a,b) represent soil characteristics at phylum and genus levels. Soil characteristics are labelled in red arrow and microbial species are labelled in green arrow.
Figure 7. Redundancy analysis of soil fungal community structure on soil characteristics (AN, AP, AK, pH, ACa and BK) in different samples. (a,b) represent soil characteristics at phylum and genus levels. Soil characteristics are labelled in red arrow and microbial species are labelled in green arrow.
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Table
Table 1. Effects of forestland conversion to tea gardens on alpha-diversity indices of soil fungi.
Table 1. Effects of forestland conversion to tea gardens on alpha-diversity indices of soil fungi.
Soil Depth/cmLand-Use TypesSobsShannonSimpsonACEChao1
0–20 cmFDA1024.33 ± 62.17 Aa3.98 ± 0.21 Aa0.07 ± 0.01 Aa1164.86 ± 81.69 Aa1144.13 ± 62.95 Aa
ZC3A545.33 ± 29.5 Ac3.81 ± 0.36 Aa0.07 ± 0.02 Aa560.28 ± 36.22 Ac558.99 ± 34.59 Ac
ZC30A665 ± 46.03 Ab3.82 ± 0.36 Aa0.07 ± 0.02 Aa729.15 ± 44.3 Ab732.4 ± 42.39 Ab
20–40 cmFDB763.66 ± 71.84 Ba3.29 ± 0.49 Bb0.13 ± 0.08 Aa906.68 ± 82.26 Ba902.3 ± 74.68 Ba
ZC3B442.33 ± 125.11 Ab3.99 ± 0.30 Aa0.04 ± 0.01 Bb452.99 ± 127.94 Ab462.29 ± 127.85 Ab
ZC30B406.66 ± 83.24 Bb3.26 ± 0.21 Bb0.10 ± 0.02 Aa429.81 ± 98.21 Bb434.66 ± 87.66 Bb
Land-use types(L)50.32 **1.78 NS1.94 NS69.29 **75.71 **
Depth(D) L × D 33.54 **4.90 *1.18 NS31.03 **33.22 **
2.12 NS2.89 NS2.21 NS2.15 NS2.65 NS
Note: Values are given as the means ± standard errors (n = 3). Different lowercase letters indicate significant differences between different soil samples of the same depth at the p < 0.05 level, and different capital letters indicate significant differences between different soil depths of the same sample at the p < 0.05 level. NS, not significant; * p < 0.05; ** p < 0.01.
Table
Table 2. Differences in the soil fungal communities examined by PERMANOVA.
Table 2. Differences in the soil fungal communities examined by PERMANOVA.
R2p Value R2p Value
FungiTopsoil (0–20 cm)0.0380.538FungiFD vs. ZC30.600.003
FD vs. ZC300.590.004
Subsoil (20–40 cm)ZC3 vs. ZC300.280.016
   
Table
Table 3. Network properties of soil fungal groups among forestland and tea garden samples.
Table 3. Network properties of soil fungal groups among forestland and tea garden samples.
Network FeaturesFDZC3ZC30
Edges695845873
Positive edges392509548
Negative edges303336325
Nodes989998
Network diameter887
Modularity0.2930.3290.344
Average degree14.1817.07117.816
Average path length2.8252.612.522
Average clustering coefficient0.5450.6030.611
Network density0.1460.1740.184
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Wang, F.; Chen, Y.; Yu, X.; Yu, W.; You, Z.; Yang, Z. Response of the Soil Fungal Community and Its Function during the Conversion of Forestland to Tea Plantations: A Case Study in Southeast China. Forests 2023, 14, 209. https://doi.org/10.3390/f14020209

AMA Style

Wang F, Chen Y, Yu X, Yu W, You Z, Yang Z. Response of the Soil Fungal Community and Its Function during the Conversion of Forestland to Tea Plantations: A Case Study in Southeast China. Forests. 2023; 14(2):209. https://doi.org/10.3390/f14020209

Chicago/Turabian Style

Wang, Feng, Yuzhen Chen, Xiaomin Yu, Wenquan Yu, Zhiming You, and Zhenbiao Yang. 2023. "Response of the Soil Fungal Community and Its Function during the Conversion of Forestland to Tea Plantations: A Case Study in Southeast China" Forests 14, no. 2: 209. https://doi.org/10.3390/f14020209

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