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Article

Effect of Different Mulching Practices on Bacterial Community Composition and Fruit Quality in a Citrus Orchard

by
Lei Yang
1,
Min Wang
1,
Shuang Li
1,
Jianjun Yu
1,
Yang Chen
2,
Haijian Yang
1,
Wu Wang
1,
Hao Chen
1 and
Lin Hong
1,*
1
Fruit Tree Research Institute, Chongqing Academy of Agricultural Sciences, Chongqing 401329, China
2
Biotechnology Research Institute, Chongqing Academy of Agricultural Sciences, Chongqing 401329, China
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(10), 1914; https://doi.org/10.3390/agriculture13101914
Submission received: 18 August 2023 / Revised: 19 September 2023 / Accepted: 26 September 2023 / Published: 29 September 2023
(This article belongs to the Section Crop Production)
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Abstract

:
Citrus fruit, the most abundant global fruit, is primarily concentrated in China. Mulching techniques have demonstrated a favorable effect on the soil’s hydrothermal environment, resulting in enhanced plant growth, yield, and quality. Nevertheless, the impact of mulching on the soil microbiome and fruit quality of Beni Madonna tangor (Citrus nanko × C. amakusa) remains unknown. This study aimed to examine the impact of different mulching techniques, namely traditional flat planting (CK), reflective film mulching (RM), black film mulching (BM), corn stalk mulching (CS), green film mulching (GM), and transparent plastic film mulching (TM), on the bacterial diversity, composition, cooccurrence networks, and bulk soil assembly during the ripening stage of Beni Madonna tangor. The various treatments employed in this study exhibited distinct impacts on fruit quality and soil temperature and humidity. Through comprehensively evaluating fruit quality and soil properties, it was found that RM treatment had the best effect, while CK treatment was the worst. The mulching results in a significant decrease in the Shannon indexcompared to the control group. Specifically, mulching with RM, CS, and GM led to a significant increase in Chloroflexi abundance (p < 0.05). Furthermore, the interaction complexity between bacteria was found to be lower under GM and TM treatments compared to the other mulching treatments. At the genus level, Chloroflexi exhibited a positive correlation with total soluble solid (TSS) and Vitamin C (Vc) contents, however, GP13 showed a converse result. It was determined that Chloroflexi, with a high abundance of RM, promoted an improvement in soil and fruit quality. Ultimately, it can be concluded that various mulching techniques yield distinct impacts on both the soil bacterial composition and citrus quality, with these effects being intricately linked to the core biota’s functionalities within each treatment.

1. Introduction

Soil agronomic management practices induce alterations in the physical and chemical characteristics of soil, leading to fluctuations in the microbial biomass and diversity of the soil [1]. The utilization of mulching practices mitigates soil evaporation, preserves soil moisture, curbs weed proliferation, regulates soil structure and temperature, impacts soil microorganisms, and enhances the visual appeal of soil [2,3].
Mulching materials can be categorized into three main groups: organic materials, inorganic materials, and special materials. Through research, it has been generally identified that mulching with organic materials, such as straw, wood chips, etc., can improve soil properties. Cornstalk mulch treatment exhibite a superior performance and enhances soil fertilization compared to alternative treatments [4]. Straw mulching significantly improves water use efficiency by reducing soil surface water evaporation and affects soil temperatures and crop yields [5,6,7,8]. It was demonstrated that straw mulching in arid regions improves crop yields and soil nutrient contents by protecting soil-associated water [9]. The utilization of coffee waste as a mulching film has the potential to enhance lettuce growth, the coffee waste film exhibit the ability to release endogenous bacteria into the soil and stimulate the plant and root growth of the assayed crop [10]. Mulching treatments utilizing both composted yard waste and ground wood pallets had significant effects on several key parameters, including the organic matter content, soil respiration, microbial biomass N, the soil pH, the cation exchange capacity, and essential plant nutrient concentrations [11]. Inorganic mulching materials, such as black plastic film, silver plastic film, and transparent plastic film, are commonly used in the semiarid areas of China [12]. Mulching with plastic film not only improves water use efficiency but also directly changes the soil’s biological characteristics and fertility. This is because, unlike straw mulching, the plastic film is impermeable and does not add any organic matter or nutrients [13,14]. During the maize seedling stage, organic manure application combined with plastic film mulching promotes photosynthesized C sequestration below ground and increases soil microbial activity [15]. In recent years, some new special materials have also been used to cover cropland, such as biodegradable film, gravel, newspapers, and so on. Studies have revealed that biodegradable and plastic film mulching significantly increases corn yields in semiarid areas by improving soil moisture (SM) and soil temperature (ST) [16,17]. Gravel and sand mulching affects the structure and metabolic capability of the bacterial community, thereby serving as a contributing factor to crop yield [18]. It is widely believed that biological materials can increase soil organic matter and improve environmental health. However, the cost of these materials is relatively high. Plastic films are cheap and the filming process is simple, but long-term use will have a certain negative impact on the soil structure. The applicability of special material films has not been widely proven.
Microorganisms are essential for the stability of soil ecosystems [19]. Bacteria are one of the main components of soil microorganisms, and play an important role in carbon and other nutrient cycling [20,21]. Several studies have revealed that agricultural management practices can change soil physicochemical properties, such as the organic matter content and soil moisture availability, subsequently causing a change in microecology [22,23,24]. Moreover, mulching was discovered to have an impact on soil microorganisms. For example, mulching treatments can alter the composition and functionality of microbial communities, which may have an impact on important soil processes that sustain crop yields [25]. Mulching practices can alter the soil’s physicochemical environment, such as increasing soil temperature and humidity, after this, the microbial community’s composition and diversity change with it [5,26,27]. Previous studies have primarily focused on examining the impact of individual mulching materials or models on soil microbial communities, but with limited comparative analyses conducted between different mulching materials or models.
Previous research has demonstrated that the incorporation of straw specifically promotes the proliferation of copiotrophic bacteria [28]. Chen et al. found that plastic film mulching could change the relative abundance of Gammaproteobacteria and Bacteroidetes in the opposite way [5]. Despite extensive investigations into the effects of various mulching practices on soil microbial community structures [5,26], there remains a limited understanding of the response of microbial networks to alterations in the soil environment. The application of high-throughput sequencing technology has dramatically broadened our understanding of bacterial communities in diverse ecological systems. Although this methodology is advantageous in ascertaining the proportional prevalence of distinct microbial taxa within a particular sample, it does not present insights into variations in the prevalence of targeted microbes across samples [29]. Recently, researchers have begun to employ absolute quantification 16S rRNA sequencing (16S-seq) techniques to tackle the technical challenges in this field by incorporating synthetic spike-in standard sequences [30,31]. Network analyses facilitate a deeper exploration of the enigmatic relationship between soil microorganisms. It was found that networks can be construed as a conceptual framework to identify microbial interactions and analyze niche sharing or competition between bacterial and fungal taxa at a collective level [32,33]. Consequently, a more comprehensive understanding of the involvement of microorganisms in soil microecology exchange is needed.
Simple agronomic measures could improve agricultural efficiency. In the current investigation, from June 2020 to September 2022, five mulching practices were implemented in a citrus orchard and compared with untreated soil to conduct a basic fruit quality analysis. Soil physicochemical properties and bacterial community structure were analyzed using 16S-seq technology under different treatments to explore the impact of film coverings on soil and fruit quality. In addition, we identified the associations between microbial communities under different treatments using a network analysis. We hypothesize that covering materials may affect changes in temperature and humidity in the soil, and the microbial community in the soil will also respond to these changes, leading to corresponding reactions. Our research results will provide a theoretical basis for convenient and efficient agricultural production.

2. Materials and Methods

2.1. Study Site

The experiment was conducted in an orchard located at the citrus experimental station of Baohe Village, Longhe Town, Changshou Area, Chognqing, China (106°92′ E, 29°71′ N; elevation = 295 m). The soil in this citrus orchard is silt loam. The study area is belonged to a subtropical humid monsoon climate, with annual rainfall and temperature averaging 1162.7 mm and 17.68 °C, respectively. Approximately 60% of the rainfall occurs in the autumn season (September–November). An accumulated temperature greater than 10 °C is 1200 h, and the average frost-free period is 360 days.

2.2. Experimental Design

In 2018, Beni-Madonna tangor (Citrus nanko × C. amakusa) trees were planted on Poncirus trifoliata (L.) Raf. rootstock at a density of 3 m × 5 m (675 plants ha−1). Every two rows of fruit trees were planted in the same 6 m wide ridge. In August to December of 2020 and 2021, the mulching experiment was established on 18 ridge, each ridge was 60 m and contained 20 citrus trees per row. Six mulching treatments were applied: (1) Reflective film mulching (RM), which covers the entire ridge, including inter-row and the tree line, leaving no gaps. (2) Black film mulching (BM). The laying method was the same as that of RM. (3) Interrow mulch, which consists of sere corn stalk (CS). (4) Green film mulching (GM). (5) Transparent plastic film mulching (TM). The treatment methods of (2) to (5) were the same as that of RM. (6) The control check (CK): no mulching and grass was naturally growing on the plot between the rows. The filming treatments were performed in sequence from 1 to 6, and 3 groups were repeated. There was a total of six treatments, each treatment repeated three ridges. The reflective film, black film, green film, and transparent film were made from plastic, with a thickness of 0.33 mm (Weijunbuzhibu Co., Ltd., Dongguan, China). The dried corn stalk was smashed into 2 cm pieces, where the laying thickness was 10 cm. All mulching materials were laid once a year.

2.3. Soil Sampling and Measurements

2.3.1. Sampling Strategy

In mid-December 2021, 5 sample trees were selected with the same amount of fruit and uniform growth on each ridge and holes were dug at the drip line of each sample tree to take soil samples (5 cm in diameter, 20 cm depth). The five soil samples were mixed together as one sample. The other two samples of the same treatment were obtained in the same manner on different ridges. There were 18 soil samples in total (6 treatments × 3 replicates). After visible stones and plant residues were removed from each sample, the soil samples were homogenized and immediately passed through a 1 mm sieve. Each soil sample was immediately frozen at −80 °C for DNA extraction and microbial community analysis.

2.3.2. Fruit Quality and Soil Properties Measure

Three sample trees were randomly selected from each treatment, and 5 fruits were picked from the four directions of each sample tree. A total of 15 fruits with average size and similar color were selected as samples. Each treatment was repeated 3 times, there were 3 sample trees in each replicate. Eight fruit quality indexes were determined: The single fruit weight, which was measured by an electronic balance. The vertical diameter, transverse diameter and pericarp thickness, which was measured with a vernier caliper, The total soluble solid (TSS), which was determined using a digital refractometer (PAL-1; Atago, Tokyo, Japan). Titratable acids (TA), which were determined by acid-base titration [34]. Finally, the vitamin C (Vc) content, which was determined by titration with 2,6-dichloroindophenol. Fruit shape indices were computed by dividing the vertical diameter by the transverse diameter. The soil temperature and relative humidity were measured with a soil temperature and humidity recorder every 10 min. The effect of each treatment was evaluated comprehensively using principal component analysis and the membership function method; the ranking order of six treatments was obtained.

2.3.3. The Relative and Absolute Quantification of 16S rRNA Genes

The absolute quantification of 16S rRNA genes was performed externally by Genesky Biotechnologies Inc. (Shanghai, China). A PowerSoil DNA isolation kit (MoBio, Carlsbad, CA, USA) was used to extract total genomic DNA. Briefly, two or three spike-in sequences at four different concentrations (103, 104, 105, and 106 copies of internal standards) were added to the sample DNA pools. The spike-in sequences contained conserved regions identical to those of natural 16S rRNA genes and artificial variable regions different from nucleotide sequences in the public databases, acting as an internal standard and allowing absolute quantification and comparison across samples [30]. The 16S rDNA V3–V4 region was amplified using PCR (95 °C for 2 min, followed by 27 cycles at 98 °C for 10 s, 62 °C for 30 s, and 68 °C for 30 s, and a final extension at 68 °C for 10 min) using the primers 341F (5′-CCTACGGGNGGCWGCAG-3′) and 805R (5′ GACTACHVGGGTATCTAATCC 3′), where the barcode was an eight-base sequence unique to each sample. The amplifications and sequences of the V4–V5 region was carried out by Genesk.

2.4. Illumina MiSeq Sequence Processing and Function Analysis

TrimGalore (v0.4.5; Babraham Bioinformatics, UK) and Mothur (v1.39.3 (https://www.mothur.org/, accessed on 15 January 2023) were used to remove the adaptor and primer sequences, respectively. At the opposite end, the reads were merged and filtered, and the remaining reads were then clustered into operational taxonomic units (OTUs) with a sequence similarity level of at least 97%. The OTUs were annotated, and a standard curve was established between the read count and the number of incorporated DNA copies. The absolute copy number of the bacterial OTUs can be calculated by using the read count of the corresponding bacterial OTUs. Bacterial community richness and diversity were assessed with the ACE and Shannon indices using the UPARSE pipeline [35]. The similarity between bacterial communities was estimated by principal component analysis (PCA) based on the Bray-Curtis measure. A bacterial interaction network (using Pearson correlations) was determined using OmicStudio tools (https://www.omicstudio.cn/tool, accessed on 15 January 2023), and the network map was made using Gephi 0.9.4. Raw sequencing data were deposited in the Genome Sequence Archive (https://bigd.big.ac.cn/gsa, accessed on 15 January 2023) (accession number: CRA011447). A redundancy analysis (RDA) was performed in R using the vegan packages. Functional profiles of the microbial communities in biofilm samples were predicted using PICRUSt (phylogenetic investigation of communities by reconstruction of unobserved states) [36].

2.5. Statistical Analysis

The numbers of OTUs related to bacteria used for each treatment were 2327 for the CK treatment, 1897 for the RM treatment, 1847 for the BM treatment, 1951 for the CS treatment, 1807 for the GM treatment, and 1343 for the TM treatment. Fruit quality and soil properties under different treatments were compared using one-way analysis of variance (ANOVA) in IBM SPSS Statistics (version 20; SPSS Inc., Somers, NY, USA). Significance was determined using Tukey’s test (p < 0.05), and the confidence level was 95%.

3. Results

3.1. Effects of Mulching on Fruit Quality and Soil Properties

No significant differences were observed in the indicators of vertical diameter, fruit shape, and TA among the six treatments. Fruit in green film mulching had the highest fruit weight and transverse diameter, and fruit in corn stalk mulching had the lowest. Pericarp of CK treatment were the thickest and pericarp of corn stalk mulching were the thinnest. TSS/TA was lowest in transparent plastic film mulching’s fruit and was highest in CK fruit. Notably, the corn stalk mulching treatment resulted in significantly lower weight, transverse, and thickness indicators than the CK treatment. Reflective film mulching and black film mulching treatment increased the TSS content in citrus fruits and improved the fruit quality (Table 1). Five mulching treatments exhibited an increased soil temperature and humidity compared to the control treatment (CK).
To provide a more intuitive representation of the results, the effects of mulching on fruit quality, soil temperature, and humidity were evaluated using principal component and membership function analyses (Table 2). A comprehensive evaluation of the six treatments was conducted using ten indices, excluding the fruit shape index. The findings indicate a high degree of consistency between the two evaluation methods. Both methods were ranked according to their score; the higher the ranking, the more effective the treatment. Among the six mulching methods, the reflective film mulching treatment demonstrated the most favorable outcome, while CK exhibited the worst result. However, transparent plastic film mulching and green film mulching treatments exhibited some variation in their rankings across the two methods due to transparent plastic film mulching’s lower TSS, resulting in green film mulching treatment securing the third position and transparent plastic film mulching occupying the fourth position. The comprehensive evaluation showed that reflective film mulching treatment ranked first and CK ranked sixth.

3.2. Diversity of Bacterial Communities

A total of 217,774 quality bacterial sequences were obtained from 18 samples and classified into 11,130 OTUs based on 97% sequence similarity. As shown in Figure 1, no significant difference was observed between the six treatments in the observed species, Chao1, and ACE (Abundance-based Coverage Estimator) indices. The Shannon indices were significantly lower in black film muiching and transparent plastic film mulching than in CK. The Simpson indices increased significantly in black film muiching compared to CK. Mulching treatments reduced the diversity of soil bacteria.

3.3. The Composition and Network of Soil Bacterial Communities Changed under Different Mulching Treatments

As can be seen from Figure 2, compared with relative quantification, absolute quantification could better reflect the influence of total bacteria and abundance of species under each treatment. Through absolute quantification of 16S rRNA genes, significant differences in the total abundance of bacteria among the six treatments were revealed, with CS exhibiting the highest abundance and BM exhibiting the lowest. We analyzed the relative and absolute abundances of soil bacteria in the six treatments at the phylum (Figure 2A,B) and genus (Figure 2C,D) levels. The soil bacteria belonged to 26 phyla and 411 genera. Species with relative abundances greater than 1% were included in the bar chart. Proteobacteria (mean abundance of the six treatments, 31.83%), Acidobacteria (25.03%), Actinobacteria (16.10%), Chloroflexi1 (10.39%), Planctomycetes (4.14%), candidate division WPS-1 (2.89%), Firmicutes (2.49%), Bacteroidetes (1.78%), candidate division WPS-2 (0.86%), and Gemmatimonadetes (0.75%) were the top 10 phyla in the bacterial communities across treatments. Notably, Chloroflexi abundance increased significantly after mulched RM, CS, or GM treatment (p < 0.05) when compared to the CK treatment. Furthermore, Bacteroidetes abundance was found to be the lowest in the GM treatment but the highest in the CK treatment. In CK treatment, the abundance of Bacteroidetes was 4.87 times higher than the average level of the TM, GM, CS, RM and BM.
There were 24 genera with relative abundances greater than 1%, except Unassigned and No Rank. The abundances of the top 10 bacterial genera across the six treatments were Gp2 (0.59%), Mizugakiibacter (0.46%), Pseudomonas (0.45%), Acidipila (0.38%), Gp13 (0.32%), WPS-1 genera incertae sedis (0.29%), Granulicella (0.22%), Gp3 (0.18%), Gp1 (0.15%), and Rhizomicrobium (0.13%). Significant differences were observed in the abundances of Gp2 and Gp13 among the six treatments, and mucilaginibacter abundance was significantly different among the six treatments (p < 0.001). In the six treatments, the abundance of bacterial genera ranged from high to low as follows: CK (572,057), CS (113,125), RM (54,670), BM (28,088), TM (19,370), and GM (12,609).
According to the PCA results, samples subjected to CK, BM, and TM treatments exhibited close clustering, while those subjected to RM, CS, and GM treatments exhibited close clustering, albeit separated by a certain distance (Figure 3). The ANOSIM analysis based on the unweighted UniFrac matrix further confirmed significant differences in the community structure among all six treatments (R = 0.376, p = 0.004). Notably, CS, RM and GM samples were found to be distinct from the CK samples, and significant variation was observed between the three samples in the BM and TM treatments individually. Overall, CK exhibited greater independence in comparison to the other treatments.
A study of the top 40 bacterial species at the genus level via a network analysis revealed that mulching treatments had an impact on bacterial group interrelationships in the soil (Figure 4). The primary microbial groups identified in this study were predominantly Acidobacteria, Proteobacteria, and Actinobacteria. There were 40 nodes and 57 edges in RM_CK, 37 nodes and 76 edges in BM_CK, 36 nodes and 78 edges in CS_CK, 35 nodes and 55 edges in GM_CK, and 36 nodes and 59 edges in TM_CK. These results indicate that the interaction network in RM_CK, GM_CK, and TM_CK was less complex than that in BM_CK and CS_CK. However, the complexity of bacterial interactions in RM_CK was found to be heightened, with a decrease in the centrality of Acidobacteria and an increase in that of Proteobacteria in BM_CK and TM_CK. Overall, the complexity and average degree of the interaction network decreased in GM_CK and TM_CK compared to the other groups.

3.4. Relationships between the Bacterial Communities and Fruit Quality or Soil Properties

Pearson correlation analyses revealed significant correlations between certain fruit quality indices and soil physicochemical properties with the abundance of dominant phyla (Figure 5A, Table S1) and genera (Figure 5B, Table S2). Notably, Chloroflexi exhibited positive correlations with TSS, Vc, and SH (soil moisture) at the phylum level, while Firmicutes and Bacteroidetes exhibited a negative correlation with ST (soil temperature) at the phylum level. At the genus level, Gp2 was positively related to TSS and SH, while Burkholderia and Acidobacterium were negatively related with ST and Acidobacterium exhibited a negative correlation with SH. Notably, Gp13 exhibited negative correlations with TSS, TA, Vc and ST.
The RDA (Redundancy analysis) results indicated that at the phylum level, the impact of environmental factors on microbial species ranged from high to low as follows: SH > ST > Vc > TSS > TSS/TA > weight > VD (Vertical diameter) > TD (Transverse diameter) > TA (Figure 6). RM exhibited a positive correlation with SH, ST, Vc, TSS, TSS/TA, and TA, while CK displayed a negative correlation with SH, ST, Vc and TSS. Nevertheless, the relationship between the remaining treatment samples and environmental factors were inconsistent. TSS/TA was positively correlated with the top 8 most abundant bacterial phyla. The results indicated a positive correlation between TSS and Acidobacteria, Actinobacteria, Chloroflexi, Planctomycetes, and WPS-1 and a negative correlation between TSS and Proteobacteria, Firmicutes, and Bacteroidetes. Vc, ST, and SH were found to be positively correlated with Actinobacteria, Chloroflexi, and WPS-1 but negatively correlated with Proteobacteria, Firmicutes, and Bacteroidetes. Acidobacteria and Planctomycetes exhibited a positive correlation with Vc and SH but a negative correlation with ST.
At the genus level, the forces of environmental factors on microbial species ranged from large to small as follows: ST > SH > TSS > TSS/TA > Vc > TD > weight > TA > VD. CK was negatively correlated with Vc, ST, and SH, while RM and GM were positively correlated with SH and ST and negatively correlated with TA. TM showed correlation with none of the soil and fruit indices. BM was negatively correlated with TA. CS was positively correlated with ST. In addition, the relationships between the other treatment samples and environmental factors were inconsistent.
TSS/TA was positively correlated with all the top 8 most abundant bacterial species. TSS was positively correlated with Acidobacteria, Actinobacteria, Chloroflexi, Planctomycetes, and WPS-1, and TSS was negatively correlated with Proteobacteria, Firmicutes, and Bacteroidetes. Vc, ST and SH were positively correlated with Actinobacteria, Chloroflexi and WPS-1 and were negatively correlated with Proteobacteria, Firmicutes, and Bacteroidetes. Acidobacteria and Planctomycetes were positively correlated with Vc and SH and negatively correlated with ST.

3.5. Prediction of the Functional Potential of Soil Bacterial Communities

Based on KEGG, KO, COG, and Metacyc databases, a total of 184, 7370, 4207 and 423 functions were annotated, respectively. Among these, 3, 729, 309, and 28 functions exhibited significant differences across various treatments. As shown in the first part of the results, through a comprehensive evaluation of soil and fruit quality indexes using two mathematical methods, the results showed that RM was the best and CK was the worst. Subsequent screening, based on various functions, indicated that the maximum value appeared in RM and the minimum value appeared in CK, yielding a total of 75 bacterial functional groups (Figure 7). An analysis of soil microorganisms in the RM revealed a number of functions related to glucose metabolism, energy metabolism, and amino acid synthesis and transport. Combined with the RDA results, it is possible to infer that the functions of Chloroflexi may be associated with the promotion of soil activity and the facilitation of sugar absorption and transport in fruits. However, the presence of GP13 is not conducive to the accumulation of glycol acids in citrus fruits.

4. Discussion

4.1. Mulching Practices Contribute to Fruit Quality and Soil Properties

Maintaining a stable and favorable soil environment is of the utmost importance in order to achieve optimal plant growth and yield quality. Soil provides the most basic ecological conditions for plant growth. The agricultural sector has been significantly impacted by rising global temperatures, leading to changes in water and energy consumption [37]. Therefore, it is very essential to take the necessary agricultural measures to maintain and improve the soil environment, which promotes plant growth and improves the quality of crops. The total soluble solids (TSS) and titratable acidity (TA) of citrus fruits serve as crucial indicators of their quality. Research has demonstrated that the application of film coatings has the potential to enhance the sugar content of ‘Wenzhou’ tangerines, ‘Valencia’ sweet oranges and other citrus varieties. In the present study, it was observed that the black film mulching and reflective film mulching treatments resulted in a significant increase in TSS content in Beni-Madonna tangor fruit, while the transparent plastic film mulching treatment showed the lowest TSS content. This result revealed that the effect of different mulching materials on citrus’s TSS was inconsistent. Previous research has indicated substantial variations in the impact of film mulching on the organic acid content of fruits [38]. However, in our study, no significant differences were observed in the TA content following different treatments, which can be attributed to the specific characteristics of the materials employed in this investigation. Mulching application resulted in the development of water stress and subsequent water deficit stress, which triggered an osmotic regulation mechanism. This mechanism ultimately led to an increase in sugar content within the fruit. Furthermore, we hypothesize that, in our study, reflective film mulching could effectively raise the TSS of fruits because the implementation of a reflective membrane to enhance illumination not only improved photosynthetic efficiency but also regulated sucrose metabolism and the activities of enzymes involved in energy substance synthesis. Consequently, this regulation promoted the accumulation of sugar and facilitated the fruit coloration process.
The effects of mulching on various aspects of soil dynamics have been extensively studied in recent research. These studies consistently demonstrate that surface mulching significantly decreases soil evaporation, alters soil temperature and moisture distribution over space and time, and modifies rainfall infiltration, runoff generation, and soil erosion processes. In a recent study by Tian et al. [39], the authors applied a random forest (RF) analysis to identify fungal alpha diversity, soil temperature, and pH as the key factors influencing broomcorn millet yield under plastic film mulching. Numerous studies have demonstrated the potential of plastic film mulching to enhance soil temperature and moisture levels [28,40,41]. It has been observed that different colored plastic films exhibit varying impacts on soil temperature and humidity. Specifically, black plastic mulch has been found to elevate soil temperature [42], whereas silver plastic mulch has been shown to reduce the soil temperature compared to uncovered soil [43]. In tropical regions, silver-colored plastic with a high reflectivity and low absorptivity and transmissivity may be a favorable choice for plants [44]. Transparent plastic film is the preferred method for soil solarization due to it causing a significant increase in soil temperature [45]. Generally, mulching treatments retain higher levels of soil moisture compared to bare soil (no mulching) [46,47]. Similarly, our research revealed significant differences among the six treatments in terms of soil temperature and soil moisture. Compared with the CK treatment, black film had the largest increase in soil temperature, while the reflective film was the most conducive to an increase in soil moisture. Furthermore, mulching can also impact the soil pH, total nitrogen, and organic carbon [48,49]. In a follow-up study, we aim to determine more physical and chemical soil indicators to reveal the impact of film mulching on the soil environment.

4.2. Mulching Practices Change the Soil Bacterial Composition and Network

Numerous studies have examined the impact of mulching film on soil bacteria diversity [50,51]. The impacts of various mulching materials and techniques on bacterial community composition and relative abundances of specific bacterial taxa were found to be significant in a study conducted by Tian et al. [39]. The effect of film mulching on soil bacterial diversity varied across different studies, with varying outcomes observed for different diversity indices. Certain studies indicated that mulching led to a reduction in bacterial α-diversity and phylogenetic diversity, as evidenced by the Shannon and Simpson indices [52,53]. Conversely, other studies reported an increase in bacterial diversity as a result of mulching [48,54,55,56,57]. Some research has shown that the application of wheat straw mulching treatments results in a decrease in bacterial community α-diversity; conversely, mulching treatment involving the seed cake of Camellia oleifera does not have a significant impact. Additionally, the use of gravel and sand for mulching was found to affect the soil bacterial community, with a higher richness and diversity observed in the mulching samples [15,58]. In our investigation, the observed, ACE, and Chao1 indices did not exhibit any noteworthy variations among the six coverage treatments. However, significant disparities were observed in the Shannon and Simpson indices. Following the application of mulching treatment, the Shannon index exhibited a decrease compared to the control, while the Simpson index exhibited an increase. These findings suggest that mulching treatment effectively diminishes the species diversity within the bacterial community present in orchard soil.
The influence of mulching on the dominant taxa and their abundance was examined. In this study, bacterial species in each mulch treatment were further annotated at the phylum and genus classification levels. The dominant soil populations identified under each treatment were Proteobacteria, Acidobacteria, and Actinomycete. The predominant bacteria observed in our study were primarily classified as Gp2. While, in the other researches, the dominant phyla identified in all soil samples were Proteobacteria, Acidobacteria, and Actinobacteria [5,57,59,60,61]. A statistical analysis revealed significant differences in the ratios of these dominant phyla among the various treatments [5]. Specifically, our research found that mulching treatment resulted in a significant decrease in the abundance of Proteobacteria and a significant increase in the abundance of Actinobacteria compared to the control group. The CS treatment led to a reduction of 39.82% in the abundance of Proteobacteria, while the BM treatment resulted in a 74.97% increase in the abundance of Actinobacteria. Liu found that application of milk vetch mulching resulted in a significant increase in the relative abundance of Actinobacteria and Chloroflexi within the bacterial community, while the relative abundances of Acidobacteria, Firmicutes, Verrucomicrobia, and Gemmatimonadetes were significantly decreased in both wheat rhizosphere and nonrhizosphere soil [62]. However, contrary to these findings, several studies have reported the opposite trend. Specifically, bacterial richness and diversity in the soil were significantly enhanced following mulching treatments compared to those observed after rotary tillage without mulching treatment. In the study conducted by Li et al. [4], it was observed that under mulching conditions, the relative abundances of Proteobacteria, Actinomycetes, TM7, and Bacteroides were found to be higher compared to the control treatment. On the other hand, plastic film mulching treatment, as reported by Luo et al. [50], resulted in a significant decrease in the relative abundances of Chloroflexi, Planctomycetes, and Verrucomicrobia, while significantly increasing the relative abundance of Proteobacteria. Furthermore, with respect to bacterial communities, straw mulching was found to increase the relative abundances of Proteobacteria, Bacteroidetes, and Acidobacteria, while reducing those of Actinobacteria, Chloroflexi, and Cyanobacteria [60]. At the phylum level, the study conducted by Zhang et al. found a significantly higher relative abundance of Nitrospirae within bacterial communities in peanut hull mulching soils compared to polyethylene film mulching soils [63]. Furthermore, Nyamwange et al. observed that mulch application led to an increase in bacterial and actinobacterial colony-forming units (CFUs) when compared to conventional tillage and inorganic fertilizers [64]. Additionally, multiple studies [57,65,66] have suggested that mulching practices may not have a significant impact on the overall bacterial and fungal diversity in bulk soil. Such diverse research results could be due to a variety of factors, such as differences in natural conditions in the experimental area, differences in plant species, and different mulching methods. It can be seen that the influence of the film coating on the core taxa is complex and diverse. Our β-diversity analysis revealed distinct variations in the species composition and community structure of soil bacteria across the six treatments. Specifically, RM, CS, and GM exhibited a higher degree of similarity, whereas BM and TM displayed closer associations. Conversely, CK demonstrated relative independence. Consequently, it can be concluded that the implementation of mulching treatment significantly impacted the species composition and community structure of soil bacteria.
Microbial network analyses enable the identification of key species and their significance within the network, potentially influencing the structure and function of the microbial community [67]. The application of various mulching treatments resulted in alterations to the soil bacterial network. Specifically, the use of plastic mulching (PM) led to a reduction in complexity and stability, as evidenced by a decrease in the number of nodes, edges, ACC, and degrees. Furthermore, the impact of PM on bacterial and fungal keystone taxa has been observed [39]. Similarly, numerous studies have demonstrated that mulching leads to a decrease in the intricacy of soil bacterial networks. However, Luo et al. discovered that plastisphere communities in sprinkling irrigation and vegetable planting systems displayed a more intricate and stable ecological network [68]. Molecular ecological network analyses unveiled that straw mulching resulted in a reduction in both bacterial and fungal network complexity [49,65,69], while simultaneously increasing the ratios between positive and negative links [34]. Zhao et al. observed that while interspecific bacterial interactions were attenuated in ridge furrows via plastic film mulching, there was an enhancement in bacterial activity and a modification of the bacterial community structure [28]. The dominant members of the microbial community under mulching were Actinobacteria, Acidobacteria, Firmicutes, Chloroflexi, Gemmatimonadetes, and Bacteroidetes, as reported by Tian et al. [65] and Zhang et al. [70]. In this study, the application of the RM treatment resulted in an increase in the number of nodes, while both BM and RM treatments led to an increase in the number of edges. Notably, a shift in the keystone microbial species from Proteobacteria to Acidobacteria was observed when comparing the effects of RM and BM treatments with each other. In a broader context, BM and CS treatments led to heightened levels of ecological network complexity and stability. Our results are generally consistent with those of previous studies.

4.3. Relationship between Soil Microorganisms and Environmental Factors or Fruit Quality after Mulching

The combination of plastic film mulching and a buried straw layer (P + S) demonstrated the highest favorability for culturable bacteria, actinomyces, and fungi, and also resulted in the highest diversity of bacterial genera when compared to alternative tillage methods. The findings also revealed significant positive correlations between soil temperature and the abundance of bacteria, Actinomycetes, and fungi. Conversely, soil water exhibited weak correlations with all of the microbial populations [66]. However, a study conducted by Yang et al. demonstrated a significant increase in soil moisture due to the implementation of mulching practices [59]. Our findings, as determined through Pearson’s correlation and RDA, revealed a positive correlation between Chloroflexi and TS, Vc content in fruit, and soil humidity. Among the six treatments examined, the abundance of Chloroflexi was found to be highest in the RM treatment and lowest in the CK treatment. In the realm of microbial function prediction, after RM treatment, soil microorganisms exhibit various functions associated with glucose metabolism and energy metabolism. Consequently, it is plausible that the functions of Chloroflexi may be linked to an increase in soil activity, as well as the absorption and transportation of sugars in fruits. At the genus level, GP13 displayed an inverse correlation with the concentrations of TSS, TA, and Vc in fruits. CK and TM treatments exhibited an absolute abundance of GP13 that was 1.52~5.58 times higher compared to RM, BM, CS, and GM treatments. Conversely, CK and TM treatments led to lower levels of TSS, TA, and Vc. These findings suggest that the presence of GP13 may hinder the accumulation of glycol acids in citrus fruits.
The utilization of flat plastic firm mulching has been identified as a viable strategy for enhancing the diversity and abundance of soil bacteria, consequently contributing to the potential stabilization of soil biological processes [55]. The application of biomulching significantly alters the structure and function of the soil microbial community within the rhizosphere of wheat plants [62]. Moreover, the implementation of black plastic geotextile fabric has been shown to enhance both chemical and biochemical soil fertility, resulting in increased orange yields in mulched soil [71]. Mulching led to an increase in bacterial functional features, specifically those associated with amino acid transport and metabolism, as well as energy production and conversion [63]. Additionally, the plastisphere exhibited enhanced predicted pathways related to human diseases, as well as the metabolism of cofactors, vitamins, amino acids, and xenobiotic biodegradation. This was accompanied by an elevation in the abundance of genes associated with carbon, nitrogen, and phosphorus cycles [50]. According to Ji et al. [72], the utilization of plastic film mulching in paddy fields serves as a proficient approach for managing and reducing CH emissions. This technique effectively regulates the composition and organization of methanogenic archaeal and fermenting bacterial communities.

5. Conclusions

This study significantly enhances our understanding of the impacts of various mulching materials on soil ecology and citrus quality. A thorough assessment of soil and fruit physicochemical indices after six treatments revealed that RM achieved the best results while CK achieved the worst. Mulching treatments resulted in a decrease in the Shannon index of soil bacteria and a modification of the community structure. The application of RM to soil resulted in increasing of Chloroflexi and reducing GP13, which were functional bacteria associated with sugar metabolism and energy metabolism, thereby enhancing agricultural productivity. Ultimately, the conclusion can be draw that various mulching techniques exert diverse impacts on soil composition and citrus quality. We suggest that a reflective film is used in citrus orchards to change soil properties and improve fruit quality.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture13101914/s1. Table S1: Correlations between certain fruit quality indices and soil physicochemical properties and the abundance of dominant phyla; Table S2: Correlations between certain fruit quality indices and soil physicochemical properties and the abundance of dominant genera.

Author Contributions

Conceptualization, L.Y. and L.H.; methodology, L.Y. and M.W.; software, M.W.; formal analysis, J.Y.; investigation, L.Y., M.W., S.L., J.Y. and L.H.; data curation, L.Y., M.W., Y.C. and W.W.; writing—original draft preparation, L.Y., S.L. and Y.C.; writing—review and editing, H.Y., H.C. and L.H.; visualization, M.W. and Y.C.; funding acquisition, L.Y. and L.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by special funds for municipal financial Scientific Research Project of Chongqing Academy of Agricultural science (cqaas2023sjczhx015) and the 2022 Citrus Industry Cluster of the Ministry of Agriculture and Rural Affairs of China (ACL202235).

Institutional Review Board Statement

“Not applicable” for studies not involving humans or animals.

Informed Consent Statement

“Not applicable” for studies not involving humans.

Data Availability Statement

Raw sequencing data were deposited in the Genome Sequence Archive (https://bigd.big.ac.cn/gsa, accessed on 15 June 2023) (accession number: CRA011447).

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Appendix A

Table A1. Abbreviated letter correspondence table.
Table A1. Abbreviated letter correspondence table.
No.Full MeaningAbbreviation
1Reflective film mulchingRM
2Black film mulchingBM
3Corn stalk mulchingCS
4Green film mulchingGM
5Transparent plastic film mulchingTM
6Total soluble solidsTSS
7Total acidityTA
8Vitamin CVc
9Redundancy analysisRDA
10Vertical diameterVD
11Transverse diameterTD
12Soil temperatureST
13Soil humiditySH
14Abundance-based Coverage EstimatorACE
15Principal component analysisPCA
16Random forestRF
17Plastic mulchingPM

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Figure 1. Alpha diversity indices of the soil bacterial community in CK, RM, BM, CS, GM and TM. Lowercase letters on the column represent the difference was significant at p < 0.05 level.
Figure 1. Alpha diversity indices of the soil bacterial community in CK, RM, BM, CS, GM and TM. Lowercase letters on the column represent the difference was significant at p < 0.05 level.
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Figure 2. Relative and absolute abundance of the abundant bacterial at phyla (A,B) and genera (C,D) among the six treatments. (CK, control group; RM, reflective film mulching; BM, black film mulching; CS, corn stalk mulching; GM, green film mulching; TM, transparent plastic film mulching. BRC1 was a bacterial phyla and Gp1, Gp2, Gp3, Gp13 were names of bacterial genera).
Figure 2. Relative and absolute abundance of the abundant bacterial at phyla (A,B) and genera (C,D) among the six treatments. (CK, control group; RM, reflective film mulching; BM, black film mulching; CS, corn stalk mulching; GM, green film mulching; TM, transparent plastic film mulching. BRC1 was a bacterial phyla and Gp1, Gp2, Gp3, Gp13 were names of bacterial genera).
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Figure 3. Principal component analysis (PCA) plot derived from Euclidean distance metrics of bacterial communities.
Figure 3. Principal component analysis (PCA) plot derived from Euclidean distance metrics of bacterial communities.
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Figure 4. Interaction networks of dominant taxa of the bacterial community at the genus level (top 40) among the six treatments. Different colors indicate the corresponding taxonomic assignments at the phylum level. The edge colors represent positive (red) and negative (green) correlations. Only significant interactions are shown (r > 0.6; p < 0.05).
Figure 4. Interaction networks of dominant taxa of the bacterial community at the genus level (top 40) among the six treatments. Different colors indicate the corresponding taxonomic assignments at the phylum level. The edge colors represent positive (red) and negative (green) correlations. Only significant interactions are shown (r > 0.6; p < 0.05).
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Figure 5. Pearson’s correlation coefficients among fruit quality, soil physicochemical properties, and abundant phyla (A) or genera (B). * p < 0.05, ** p < 0.01, *** p < 0.001. Correlation coefficients and p-values are presented in the Tables S1 and S2.
Figure 5. Pearson’s correlation coefficients among fruit quality, soil physicochemical properties, and abundant phyla (A) or genera (B). * p < 0.05, ** p < 0.01, *** p < 0.001. Correlation coefficients and p-values are presented in the Tables S1 and S2.
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Figure 6. RDA (Redundancy analysis) among fruit quality, soil physicochemical properties and abundant phyla (A) or genera (B).
Figure 6. RDA (Redundancy analysis) among fruit quality, soil physicochemical properties and abundant phyla (A) or genera (B).
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Figure 7. Predicted functions of the bacterial community across treatments.
Figure 7. Predicted functions of the bacterial community across treatments.
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Table 1. Fruit quality and soil properties for six mulching treatments.
Table 1. Fruit quality and soil properties for six mulching treatments.
Weight (g)Vertical Diameter (mm)Transverse Diameter (mm)Fruit Shape IndexThickness
(mm)		TSS (%)
CK182.67 ± 20.12 a62.4 ± 2.38 a73.27 ± 2.95 a0.85 ± 0.01 a2.70 ± 0.11 a11.37 ± 0.48 ab
CS149.67 ± 1.86 b60.03 ± 1.07 a68.27 ± 0.19 b0.88 ± 0.02 a1.99 ± 0.14 c11.23 ± 0.33 ab
TM180.00 ± 0.58 a64.27 ± 0.80 a72.33 ± 0.55 ab0.89 ± 0.02 a2.27 ± 0.04 bc10.53 ± 0.12 b
BM166.33 ± 8.74 ab61.23 ± 1.09 a71.30 ± 1.4 ab0.86 ± 0.01 a2.23 ± 0.09 bc11.73 ± 0.19 a
RM177.33 ± 1.76 ab62.43 ± 0.38 a72.87 ± 2.33 a0.86 ± 0.01 a2.06 ± 0.06 bc11.60 ± 0.20 a
GM183.33 ± 2.60 a63.67 ± 1.03 a73.57 ± 0.46 a0.87 ± 0.01 a2.33 ± 0.09 b11.10 ± 0.23 ab
TA (%)TSS/TAVc
(mg/100 mL)		Soil Temperature (°C)Soil humidity (%)
CK0.89 ± 0.04 a12.77 ± 0.03 a27.47 ± 2.87 b19.84 ± 1.51 d24.27 ± 1.04 c
CS0.90 ± 0.05 a12.47 ± 0.32 ab31.58 ± 0.55 ab25.68 ± 1.91 bc34.71 ± 4.08 ab
TM0.88 ± 0.02 a11.96 ± 0.14 c30.53 ± 0.53 ab26.50 ± 1.60 c30.12 ± 2.25 b
BM0.96 ± 0.05 a12.23 ± 0.44 bc32.63 ± 0.53 a29.42 ± 1.14 a31.38 ± 4.23 b
RM0.94 ± 0.02 a12.34 ± 0.05 abc33.16 ± 0.91 a26.11 ± 2.04 bc37.98 ± 1.97 a
GM0.89 ± 0.01 a12.47 ± 0.12 ab32.63 ± 0.76 a27.87 ± 2.16 ab31.80 ± 1.74 b
Note: CK, control group; RM, reflective film mulching; BM, black film mulching; CS, corn stalk mulching; GM, green film mulching; TM, transparent plastic film mulching; TSS, total soluble solids; TA, total acid. Lowercase letters after numbers in the same column represent the difference was significant at p < 0.05 level. All abbreviations represent the meaning in Table A1. The same as below.
Table 2. Comprehensive evaluation of the six mulching treatments.
Table 2. Comprehensive evaluation of the six mulching treatments.
Principal Component AnalysisMembership Function MethodFinal
Ranking
Factor 1Factor 2Factor 3ScoreRankU1U2U3ScoreRank
CK−3.42−1.670.72−2.1560.000.000.710.1166
CS1.26−1.28−1.92−0.0650.830.100.000.4055
TM−1.172.48−0.71−0.0540.401.000.320.4834
BM1.63−0.760.010.6520.890.220.520.5422
RM2.250.251.821.6011.000.461.000.7311
GM−0.540.980.080.0130.510.640.540.4743
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MDPI and ACS Style

Yang, L.; Wang, M.; Li, S.; Yu, J.; Chen, Y.; Yang, H.; Wang, W.; Chen, H.; Hong, L. Effect of Different Mulching Practices on Bacterial Community Composition and Fruit Quality in a Citrus Orchard. Agriculture 2023, 13, 1914. https://doi.org/10.3390/agriculture13101914

AMA Style

Yang L, Wang M, Li S, Yu J, Chen Y, Yang H, Wang W, Chen H, Hong L. Effect of Different Mulching Practices on Bacterial Community Composition and Fruit Quality in a Citrus Orchard. Agriculture. 2023; 13(10):1914. https://doi.org/10.3390/agriculture13101914

Chicago/Turabian Style

Yang, Lei, Min Wang, Shuang Li, Jianjun Yu, Yang Chen, Haijian Yang, Wu Wang, Hao Chen, and Lin Hong. 2023. "Effect of Different Mulching Practices on Bacterial Community Composition and Fruit Quality in a Citrus Orchard" Agriculture 13, no. 10: 1914. https://doi.org/10.3390/agriculture13101914

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