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Article

Land Use Rather than Microplastic Type Determines the Diversity and Structure of Plastisphere Bacterial Communities

by
Yangyang Wang
1,2,
Zixuan Zhang
1,2,
Shuang Zhang
1,2,
Wanlin Zhuang
1,2,
Zhaoji Shi
1,2,
Ziqiang Liu
1,2,
Hui Wei
1,2,3 and
Jiaen Zhang
1,2,3,*
1
Guangdong Engineering Technology Research Centre of Modern Eco-Agriculture and Circular Agriculture, Key Laboratory of Agro-Environment in the Tropics, Ministry of Agriculture and Rural Affairs, South China Agricultural University, Guangzhou 510642, China
2
Department of Ecology, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
3
Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou 510642, China
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(7), 778; https://doi.org/10.3390/agriculture15070778
Submission received: 21 February 2025 / Revised: 17 March 2025 / Accepted: 17 March 2025 / Published: 3 April 2025
(This article belongs to the Special Issue Innovative Conservation Cropping Systems and Practices—2nd Edition)
Browse Figures
Versions Notes

Abstract

:
Microplastic (MP) pollution has raised global concerns, and biodegradable plastics have been recommended to replace conventional ones. The “plastisphere” has been considered a hotspot for the interactions among organisms and environments, but the differences in the properties of soil microbial communities in the plastisphere of conventional and biodegradable MPs remain unclear. This in situ experiment was conducted to compare the diversity and structure of the bacterial community in the plastisphere of conventional MPs (polyethylene [PE]) and biodegradable MPs (polylactic acid [PLA]) in vegetable fields, orchards, paddy fields, and woodlands. It was discovered that the bacterial α-diversity within the plastisphere was significantly lower than that in the soil across all land use. Significant differences between plastic types were only found in the vegetable field. Regarding the community composition, the relative abundances of Actinobacteriota (43.2%) and Proteobacteria (70.9%) in the plastisphere were found to exceed those in the soil, while the relative abundances of Acidobacteriota (45.5%) and Chloroflexi (27.8%) in the soil were significantly higher. The complexity of the microbial network within the plastisphere was lower than that of the soil. Compared with the soil, the proportion of dispersal limitation in the PLA plastisphere significantly decreased, with the greatest reduction observed in the vegetable field treatment, where it dropped from 57.72% to 3.81%. These findings indicate that different land use types have a greater impact on bacterial community diversity and structure than plastics themselves, and that biodegradable MPs may pose a greater challenge to the ecological function and health of soil ecosystems than conventional MPs.

1. Introduction

Plastic products have become indispensable in daily life, along with their increasing production [1], and they are also widely used in agriculture and other fields due to their low cost [2], flexibility, and durability [3,4]. The plastics in the environment generally are fragmented or degraded into smaller particles or fragments (<5 mm; microplastics [MPs]) through photodegradation [5], physical abrasion [6], and biological activities [7]. It has been estimated that the amount of MPs entering the soil is 4 to 23 times greater than that entering the ocean [8]. The existence of these MPs within ecosystems can give rise to a diverse range of far-reaching negative consequences. In aquatic ecosystems, MPs influence water quality [9]. In soil ecosystems, MPs exert notable environmental impacts by selectively enriching microbial communities with essential ecological functions [10]. Soil microorganisms, critical for nutrient cycling and pollutant degradation, may experience disrupted metabolic pathways in the presence of MPs, thereby influencing organic matter decomposition and metabolite synthesis [11]. MPs also influence the expression of microbial genes involved in the carbon, nitrogen, and sulfur cycles, thereby negatively impacting key biogeochemical processes and ecosystem stability [12]. Studies have demonstrated that MPs serve as enrichment sites for potential pathogens, which impacts disease transmission and treatment and consequently heightens environmental risk [13,14,15].
To mitigate the potential risks associated with conventional MPs, various biodegradable plastic products, such as those made by polylactic acid (PLA), poly butylene succinate (PBS), and poly butylene-adipate-co-terephthalate (PBAT), have been developed as alternatives [16]. Biodegradable plastics can be fully degraded by soil microorganisms under specific conditions, breaking down into harmless substances such as carbon dioxide and water [17,18]. However, they degrade slowly in a natural environment, often taking several years, during which MPs will also be formed due to abiotic processes and biotic activities [19]. The complete degradation of biodegradable MPs involves the colonization of soil microorganisms on its surface [20,21]. As an exogenous hydrophobic substrate, the surface of MPs can provide a unique niche for the growth of various microbial species. These microorganisms form biofilms on the surface of MPs, known as the “plastisphere” [22,23,24].
The unique characteristics of the plastisphere have attracted significant research attention. The microbial community composition and structure within the plastisphere are distinct from that of the soil environment. A study has found that, relative to surrounding soil, the plastisphere exhibits decreased relative abundances of Acidobacteriota, Chloroflexi, Gemmatimonadota, and Methylomirabilota [25]. Another study showed that plastisphere formation enhances the ability of MPs to act as carriers to absorb and carry harmful pollutants and chemicals in the environment [26]. For example, they can gather heavy metals and persistent organic pollutants [27]. When organisms ingest these MPs, the associated pollutants can be released inside the organisms, causing toxicity that disrupts normal physiological functions and hormonal balances [28]. Studies have demonstrated that the relative abundances of metabolic pathways associated with human diseases and animal pathogens are significantly elevated on microplastic surfaces compared with surrounding soil [29]. Additionally, some microorganisms in the plastisphere may play a crucial role in plastic degradation. Degrading bacteria contribute to the weathering and fragmentation of MPs, enhancing their mobility and associated ecological risks [30]. Previous studies have shown that the composition of the plastisphere microbial community is influenced by factors such as substrate type, geographical location, exposure time, and environmental conditions [31]. Although numerous studies have examined microbial communities within the soil plastisphere, limited data exist regarding these communities in both conventional and biodegradable plastispheres across different land use types. This knowledge gap may indicate the potential threats that soil plastispheres pose to human health and ecological stability. Further research is urgently needed to better understand microbial community structures in both conventional and biodegradable plastispheres across diverse soil ecosystems. Different land use patterns alter soil nutrient cycles, which, in turn, affect the biochemical characteristics of the soil and lead to changes in the microbial community structure [32,33].
An in-depth study of plastisphere microbial communities across different land use types can deepen our understanding of the complex effects of MPs on terrestrial ecosystems and provide a scientific basis for assessing their environmental risks. Most existing studies are based on laboratory simulations. In real soil environments, MPs typically do not remain in their original pristine agglomerated state. Instead, they are subject to fragmentation, degradation, and interactions with other soil components influenced by various physical, chemical, and biological factors. These transformations make it possible to restrict the interactions between soil and microplastics, as well as microbial dynamics to some extent. Bridging the gap between laboratory and real-world conditions is essential for understanding the environmental behavior and ecological risks of MPs. To address this gap, in situ incubation experiments were conducted across four land use types, utilizing glass beads (GBs) (as a control) and two types of MPs. The experiment aimed to simulate the natural degradation process of MPs and the dynamic changes in the associated microbial community, providing results closer to real-world conditions. This study examined the composition and changes in the plastisphere microbial community under different land use patterns and analyzed the variations in microorganisms between different particle types and soil environments. This in situ study offers a new perspective on the environmental behavior of MPs and their potential impacts on ecosystems across different land use environments. The objectives of this study are (1) to explore differences in plastisphere bacterial communities under various land use types, evaluating significant differences in microbial colonization compared with the control group (soil and GBs); and (2) to clarify the interactions, assembly mechanisms, and potential functions of plastisphere microbial communities. We hypothesize that (1) bacterial communities will differ significantly due to habitat variations (soil and plastisphere) and polymer types; and (2) the regulatory effects of different land use types on the plastisphere (polyethylene [PE] and PLA) are greater than those of different plastic types.

2. Materials and Methods

2.1. Qualities of MPs

In this study, conventional MPs (PE) and biodegradable MPs (PLA) were used, and both were sourced from Zhonglian Plastic Technology Co., Ltd., Dongguan, Guangdong Province, China. Additionally, GBs were selected as a common reference material found in both natural and artificial environments. All substrates had a particle size of 4 mm. The surface morphology of MPs and GBs was observed using a 3.00 kV field emission scanning electron microscope (SEM, SU8010, Hitachi, Tokyo, Japan) after gold sputtering to enhance conductivity (Figure 1). Energy-dispersive spectroscopy (EDS, HORIBA, EMAX mics2, Hitachi, Tokyo, Japan) was used to analyze the surface elements of MPs and GBs (Figure S2). Additionally, the structure of GBs and MPs (PE and PLA) was analyzed using Fourier transform infrared spectroscopy (FTIR), and the characteristic changes under different treatment conditions were examined (Figure S3).

2.2. Experimental Design

A field experiment was conducted from January 2024 to March 2024 at the Zengcheng Teaching and Research Base (113.63° E, 23.23° N) of the South China Agricultural University in Guangzhou (Figure S1). During this period, the average temperature and precipitation were 17.07 °C and 32.63 mm, respectively. Four land use types were selected for this study: vegetable field (VF), orchard (OR), paddy field (PF), and woodland (WL). In VF land use, alterations in physical structure and chemical properties occurred as results of frequent agricultural activities such as fertilization, irrigation, and plowing. In OR land use, due to long-term fruit-tree cultivation, a deep and extensive root distribution was established, which modifies the soil structure. In PF land use, unique water management practices resulted in the soil being maintained in an alternating wet–dry state. This environmental change has the potential to impact microbial growth and metabolism. When contrasted with VF, OR, and PF, WLs were subject to relatively minimal human interference, and their ecosystems were in a relatively natural and stable condition. For the initial physical and chemical properties of the soil, please refer to the Supplementary Material (Table S1).
Prior to landfilling, MPs underwent 1% sodium hypochlorite treatment (30 min) followed by three-stage sterile water rinsing until no detectable hypochlorite residuals (<0.01 ppm) remained. Due to the difficulty of directly collecting MPs from the soil, nylon mesh bags (mesh size: 40 μm) were used to contain the MPs. The nylon mesh bags were employed for the collection of MPs, owing to their excellent air permeability and ability to exert negligible influence on the composition of the bacterial community [34,35]. Every mesh bag, filled with 10 g of MPs, was buried in soil at a 20 cm depth with 10 cm spacing between bags. This setup lasted two months to facilitate the formation and stabilization of the plastisphere around the MPs. Each treatment had five replicates, spaced 10 m apart. A total of 60 samples were collected for investigation. At the end, samples of GB and MPs were carefully extracted from the mesh bags. This was carried out using sterile gloves and tools to prevent contamination. The extracted samples were then promptly collected into sterile containers. The process of extracting microplastics can refer to previous studies [36]. These containers were conveyed to the laboratory, whereupon the samples were stored at −80 °C to maintain their integrity and stability, pending further analysis.

2.3. Microplastic Collection and Treatment

In the laboratory, several precautions were implemented to prevent MPs contamination. The materials employed in the MPs pellet and GB extraction experiments were all made of glass or metal. Specifically, the stainless-steel spoons were rinsed with sterile water prior to each sampling stage. All the Petri dishes and beakers utilized during the experiments were washed three times using filtered sterile water and subsequently covered with aluminum foil after each step. The collected plastic pellets and GB were gently rinsed with sterile water to eliminate the large soil particles adhering to their surfaces and then transferred into 5 mL sterile centrifuge tubes. All samples were stored at −80 °C, and the DNA extraction was planned to be conducted within one week.

2.4. Measurement of Soil Physicochemical Properties, DNA Extraction, and Amplicon Sequencing

The essential physical and chemical characteristics of the soil were measured in strict accordance with standard procedures. The moisture content of the soil was determined using the oven drying method. The pH value of a soil–water suspension, prepared by mixing soil and water at a ratio of 1:2.5, was precisely determined using a calibrated pH meter. Dissolved organic carbon (DOC) was determined quantitatively determined through the utilization of a total organic carbon (TOC) analyzer after extraction with 0.5 mol/L K2SO4 [37]. Soil microbial biomass carbon (MBC) and nitrogen (MBN) were assessed using the chloroform fumigation-extraction method and measured with a TOC analyzer [38] with a correction coefficient of 0.45 applied. The contents of total carbon (TC) and total nitrogen (TN) in the samples were determined via a total organic carbon (TOC) analyzer. Ammonium nitrogen (NH4+-N) was determined using a UV-Vis spectrophotometer [39], and nitrate nitrogen (NO3−-N) was analyzed with a dual-wavelength spectrophotometer [40].
Microbial DNA was extracted from the soil and from the surface of the MPs using the E.Z.N.A. Soil DNA Kit (Omega Biotek, Norcross, GA, USA). The bacterial 16S ribosomal RNA gene was amplified by PCR (95 °C for 2 min, followed by 27 cycles at 95 °C for 30 s, 55 °C for 30 s, and 72 °C for 60 s, with a final extension at 72 °C for 5 min) using primers 341F (5′-CCTAYGGGRBGCASCAG-3′) and 806R (5′-GGACTACNNGGGTATCTAAT-3′), where each sample had a unique eight-base sequence barcode. PCR reactions were performed in triplicate in a 20 μL mixture containing 4 μL of 5× FastPfu Buffer, 2 μL of 2.5 mM dNTPs, 0.8 μL of each primer (5 μM), 0.4 μL of FastPfu Polymerase, and 10 ng of template DNA. Amplicons were extracted from 2% agarose gels and purified using the AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, USA). The passed sequence was duplicated and then the DADA2 algorithm was performed to identify insertion deletions and substitutions. The double-ended data were performed, with up to two expected errors per read. After the sequences were spliced and chimeras were filtered, the phylogenetic relationships of each 16S rRNA gene sequence (hereafter referred to as ASVs) were analyzed by RDP Classifier against the Silva (SSU132) 16S rRNA database using a 70% confidence threshold.

2.5. Statistical Analysis

Statistical analyses were performed using SPSS 27.0 software. For comparative analyses, one-way analysis of variance (ANOVA) was performed to compare microbial bacterial community diversity indices (Shannon and Faith’s PD) among different treatments under the same land use. Two-way ANOVA was performed to assess the main effects and interactions between different land use practices and microplastic types, with a significance level set at p < 0.05. The β-diversity of the bacterial community was graphically presented via Principal Coordinate Analysis (PCoA) founded on the Bray–Curtis distance metric. The significance was assessed using permutational multivariate analysis of variance (PERMANOVA) in the “vegan” package. Venn diagrams were used to explore the similarity and overlap of ASVs composition between samples. The “igraph” package was employed to infer networks [41], and Gephi-0.10.1 software was used to construct the network and calculate topological parameters [42]. Additionally, specificity–occupancy (SPEC-OCCU) plots were used to identify potential specialist species within the microbial community [43]. To identify specialist species for each land use, ASVs with specificity and occupancy values of 0.7 or higher were considered specific ASVs in this study. To quantify the microbial community assembly mechanisms, the iCAMP package was used to identify five assembly processes: homogeneous selection, heterogeneous selection, homogenizing dispersal, dispersal limitation, and drift [44]. Furthermore, the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway was used to determine the functional gene composition of bacteria, while the Functional Annotation of Prokaryotic Taxa (FAPROTAX) was employed to identify functional groups associated with specific metabolic phenotypes.

3. Results

3.1. Surface Morphology of Glass Ball and Microplastics

SEM analysis showed that the surface morphology of GBs and PE remained unchanged after two months of burial in soil, maintaining a smooth appearance with no dents (Figure 1a,b), whereas the surface of PLA MPs became rough, exhibiting pores, cracks, and irregular pits (Figure 1c). EDS analysis was utilized to precisely determine the compositional data of the chemical elements present on the surfaces of GBs and MPs, with the detected elements encompassing C, O, Na, Al, Si, K, Ca, and Ba. The glass bead surfaces exhibited relatively higher proportions of Si and O elements (Figure S2a,d,g,j). A comparative analysis of the elemental composition between PE and PLA MPs revealed distinct chemical signatures: PE demonstrated predominant carbon (C) enrichment (Figure S2b,e,h,k), whereas PLA MPs displayed enhanced oxygen (O) content (Figure S2c,f,i,l). Under different land use conditions, the FTIR absorption peaks of the three substrates primarily varied within the range of 4000–400 cm−1 (Figure S3). GBs exhibited a robust absorption peak at 1600 cm−1, attributable to the stretching vibration of C=C. PE presented strong absorption peaks at 2900 and 2800 cm−1 due to the stretching vibration of C-H. PLA MPs showed strong absorption peaks at 3400 and 3300 cm−1, originating from the stretching vibration of O-H.

3.2. Bacterial Community Diversity and Composition

Shannon and Faith’s PD indices of soil bacterial communities in VF and PF land use were significantly higher than those in OR and WL land use (Figure 2a,b). The α-diversity of GBs and the plastisphere (PE and PLA) was significantly lower compared with soil. In the VF land use, the bacterial diversity of the PE plastisphere was significantly lower in contrast to that of GBs and the PLA plastisphere. The analysis of β-diversity demonstrated a distinct segregation of microbial communities in the plastisphere along the PC1 axis from those in soil (R2 = 0.62, p = 0.001) (Figure 2c,d), while there was no separation between PE and the PLA plastisphere. Two-way ANOVA revealed significant interactive effects of land use type and substrate type on α-diversity and Bray–Curtis (p < 0.05). The number of unique ASVs was higher than the number of ASVs common to all samples for all four land uses. For the plastisphere, the number of unique ASVs in the PLA plastisphere was higher than the number of unique ASVs in the PE plastisphere. In addition, the highest number of unique ASVs in the plastisphere was observed in the PF land use treatment (Figure S4).
Under different land use types, there are significant differences in the bacterial compositions of soil and the plastisphere (PE and PLA) at the phylum and family classification levels (Figure 3 and Figure S5). Compared with soil, the dominant phyla Proteobacteria (35.1–70.9%) and Actinobacteriota (13.1–43.2%) in the plastisphere reached the highest relative abundances in the PLA plastisphere (70.9%) in the VF land use, and the PE plastisphere (43.2%) in the PF land use, respectively. In contrast, the dominant Acidobacteriota (16.3–45.5%) and Chloroflexi (19.1–27.8%) in soil had the highest relative abundances in the OR and PF land use (p < 0.05). It might be worthwhile to note that Acidobacteriota and Chloroflexi considerably decreased in relative abundance in GBs and the plastisphere. Compared with soil, the significantly enriched families in the plastisphere (PE and PLA) included Beijerinckiaceae (4.1–11.1%), Burkholderiaceae (3.4–15.0%), Rhizobiaceae (7.7–21.1%), Comamonadaceae (2.9–8.7%), and Xanthobacteraceae (11.2–19.8%). In contrast, the relative abundances of Anaerolineaceae (0.9–38.4%) and Ktedonobacteraceae (7.4–48.7%) in soil were higher than those in the plastisphere (PE and PLA) (Figure S5).
The SPEC-OCCU analysis identified specialist species in both the soil and plastisphere across different land use types (Figure 4). There was a significant difference in the number of specialist species across different land use. The greatest quantity of specialist species (184) was observed in the VF land use, followed by the PF land use (163), OR land use (89), and WL land use (80). There are 11, 11, 12, and 4 specialized species in GB, respectively. In comparison to the PLA plastisphere, the PE plastisphere harbored a greater number of specialist species, with 8, 9, 17, and 18 specialist species observed in the VF, OR, PF, and WL land uses, respectively. Most of these specialist species belonged to Actinobacteriota and Proteobacteria.

3.3. Co-Occurrence Network Characteristics of Bacterial Community

In this study, the PE plastisphere co-occurrence networks in the vegetable, orchard, rice field, and woodland treatments had 44, 47, 55, and 66 nodes and 113, 118, 224, and 221 edges, respectively. The PLA plastisphere networks had 44, 41, 48, and 41 nodes and 121, 163, 223, and 256 edges. Both the PE and PLA plastisphere networks were significantly smaller than the soil network, which had 178, 88, 147, and 72 nodes and 1853, 316, 1255, and 462 edges (Figure 5). The average degree of the PE plastisphere networks was 5.14, 5.02, 8.15, and 6.70, and that of the PLA plastisphere networks was 5.50, 7.95, 9.29, and 12.49. Both were smaller than the soil network average degree of 20.82, 7.18, 17.08, and 12.83. The plastisphere networks had fewer nodes, links, and a lower average degree than the soil network. Additionally, the plastisphere networks exhibited higher modularity and average clustering coefficients than the soil network, with the PE plastisphere network showing the highest values.

3.4. Microbial Community Assembly

In the bacterial community composition across the four land uses, DL and DR were the predominant factors, whereas heterogeneous selection played a negligible role (Figure 6). Since homogenizing dispersal, dispersal limitation, and drift were considered random processes, randomness primarily drives the composition of bacterial communities, with the average relative contribution rates ranging from 69.79% to 81.72% in VF, 60.53% to 79.35% in OR, 79.88% to 82.61% in PF, and 59.22% to 89.20% in WL. However, compared with soil, the DL ratio in the PLA plastisphere showed a marked decrease across all land use types, from 57.72% to 3.81%, 58.91% to 7.41%, 62.52% to 30.66%, and 59.79% to 14.46%, respectively.

3.5. Functions of Bacterial Community in Plastisphere

The potential functions of bacterial communities in soil and plastispheres under different land use types were predicted using KEGG and FAPROTAX databases. Compared with soil, significant differences were observed in the abundance of functional genes associated with xenobiotic biodegradation and metabolism, amino acid metabolism, lipid metabolism, carbohydrate metabolism, infectious diseases, and drug resistance in PE and PLA plastisphere across different treatments (Figure 7). Additionally, bacterial communities in the plastisphere involved in element cycles (including plastic degradation, carbon, nitrogen and sulfur) displayed varying relative abundances based on functional selection (Figure 8). Specifically, the PLA plastisphere exhibited higher relative abundances in functions such as plastic degradation, ureolysis, dark hydrogen oxidation, nitrate reduction, nitrate/nitrogen respiration, nitrogen fixation, and sulfur compound oxidation compared with the PE plastisphere. Conversely, the abundance of aromatic compound degradation and aromatic hydrocarbon degradation was greater in the PE plastisphere.

4. Discussion

4.1. Changes in Bacterial Community in Plastisphere Across Land Use

Land use types significantly influence the diversity of bacterial communities in the plastisphere of PE and PLA, as evidenced by reduced Shannon and Faith’s PD indices (Figure 2a,b). This observation is in accordance with previous research findings [45,46]. The differences in the abundance and composition of the microbial communities are explained by the variations in soil properties, plant cover types, and the intensity of land management across different land use types [47,48]. In the VF land use, frequent agricultural activities such as plowing, the application of fertilizers, and irrigation disrupt the original soil aggregate structure [49]. As a result of this disruption, the soil porosity is changed, the nutrient contents and ratios are altered, the initial nutrient balance is broken, and the soil moisture and aeration are affected [50]. Consequently, the soil microbial environment is impacted, which disturbs the initially stable microbial community structure and makes it more difficult for microorganisms to attach to and colonize the surface of the plastisphere. Secondly, the plastisphere acts as a selective “filter” for specific microorganisms, and it differs from the surrounding soil in terms of nutrient utilization, spatial distribution, and population richness [51,52]. This leads to the plastisphere having a lower-level function, being more susceptible to environmental changes or disturbances, and making it harder for microorganisms to attach to the surface of the PE plastisphere and form colonies [53,54]. Interestingly, the methods of soil disturbance in the PF land use may be more beneficial to the PLA plastisphere. For example, tillage operations that mix the soil create more suitable living spaces and conditions for resource acquisition for the PLA plastisphere. The decomposition of more organic matter in the environment can provide abundant nutrients for the PLA plastisphere, which has the potential to increase its diversity [55]. The differences in the biodegradability of MPs may also play a role in these phenomena. PE, which are mainly composed of high-energy carbon–carbon and carbon–hydrogen bonds, show strong resistance to degradation [56]. This resistance limits their interaction with the surrounding soil environment [57]. The absence of favorable conditions for microbial colonization restricts survival to microorganisms with specific tolerances, establishing a simplified microbial community structure. This simplicity further impedes microbial colonization within the PE plastisphere. In contrast, within the PF land use context, PLA, which is principally synthesized through the dehydration–condensation reaction between carboxyl (-COOH) and hydroxyl (-OH) groups [58], furnishes the microorganisms in the PLA plastisphere with more abundant resources and a more variegated environment. This, in turn, allures bacteria with diverse functions, enabling them to occupy distinct ecological niches [59,60]. These bacteria may engage in complex interactions such as symbiosis and competition, which promote the diversity of the microbial community and are favorable for the attachment of bacteria [61]. In summary, land use types serve as a significant factor influencing the diversity and structure of bacterial communities on the surfaces of plastisphere (PE and PLA). These findings provide new perspectives for understanding the ecological effects of MPs in different ecosystems and offer a scientific basis for predicting their potential environmental risks.
Plastispheres (PE and PLA) altered the abundance of dominant bacteria communities at both the phylum and family levels (Figure 3 and Figure S5). This aligns with previous studies reporting that the presence of MPs enriches specific bacteria involved in biodegradation, consequently shifting the relative abundance of Proteobacteria and Actinobacteriota [10,54,62]. Notably, in the VF land use of this study, the relative abundance of Proteobacteria was highest in the PLA plastisphere. Proteobacteria can colonize plastic surfaces early [63]. Members of this phylum play crucial roles in carbon and nitrogen metabolism, with families such as Rhizobiaceae, Burkholderiaceae, and Pseudomonadaceae utilizing specific organic compounds generated during plastic degradation, thereby dominating the plastisphere community [64,65]. Short-term cultivation experiments suggest that bacteria can adapt to plastic environments or utilize plastic-derived compounds [66]. Additionally, our study identified an enrichment of potential nitrogen-fixing bacteria in the PLA plastisphere, including Xanthobacteraceae, Comamonadaceae, and Burkholderiaceae. Among these, Comamonadaceae are known hydrocarbon degraders that synergistically interact with other organic matter-degrading microbes [67], playing a pivotal role in soil organic matter decomposition and nutrient cycling [68]. The high biodegradability of PLA MPs enables the release of lactic acid monomers or oligomers during degradation [69], creating novel growth environments and providing nutrients and energy sources for microbial colonization [70]. Furthermore, the buried PLA MPs have a rougher and drier texture compared with PE due to weathering, and there are irregular cracks on the surface and possible chemical property changes [71]. This creates favorable conditions for the colonization of heterotrophic microorganisms, especially Proteobacteria, and strongly supports their growth. Based on our research results, it is indicated that biodegradable MPs are more susceptible to physical, chemical, and biological processes compared with conventional MPs. The rough and irregular surface provides more favorable conditions for the colonization of microorganisms, which may account for the differences in bacterial communities between the PE and PLA plastisphere.

4.2. Changes in Microbial Community Co-Occurrence Network and Assembly

The microbial interaction network was further analyzed to investigate the interaction of bacteria within different substrate types and soil, which play a critical role in maintaining habitat health and functionality. The co-occurrence network of bacterial communities in plastispheres (PE and PLA) and soil exhibited consistent patterns under different land use types (Figure 5). This variation was most pronounced in the VF land use, as reflected by reductions in microbial network complexity. Meanwhile, we observed a decline in bacterial community diversity within the plastisphere. In previous studies, lower diversity likely leads to reduced network complexity, as fewer potential interactions simplify the network structures [72]. In addition, distinct co-occurrence network characteristics were exhibited by the PE and PLA plastisphere. The PE plastisphere exhibited decreases in bacterial network complexity compared with the PLA plastisphere but increases in modularity. High levels of modularity in the microbial network may indicate niche differentiation and environmental heterogeneity [73]. Conversely, microbial network complexity increased in the PLA plastisphere, aligning with findings in a previous study [74]. Based on the SEM images (Figure 1), holes, cracks, and irregular deep pits were found to be present on all surfaces of the PLA MPs. This suggests that the carbon chains of biodegradable PLA MPs are more easily broken down and utilized by microorganisms [75].
Our findings indicate that dispersal limitation and drift are the primary factors influencing bacterial community assembly (Figure 6), consistent with previous research [74]. Although stochastic processes are the main driving factors of bacterial communities, substrates can regulate the balance between deterministic and stochastic processes in microbial community assembly to a certain extent by providing resources, affecting microbial interactions and modulating diffusion [76]. In the current investigation, compared with soil, the PLA plastisphere in the VF land use reduced the proportion of diffusion limitation. This may be due to the higher biodegradability of PLA MPs, which, during degradation, disrupt microbial habitats by providing new diffusion pathways, altering environmental conditions, influencing bacterial behavior, and reducing the proportion of diffusion limitation in bacterial community assembly and increasing the importance of stochastic processes [77]. Another possible explanation is that PLA MPs degradation enhanced homogenizing dispersal [74]. In soil ecosystems, stochastic processes play a crucial role in bacterial community assembly by influencing diffusion, mutation, birth, and death events [78], which increase diversity and uncertainty in community composition [79,80]. According to a previous study, temperature changes led to changes in microbial community assembly [81]. In addition, when the microbial community diversity was low, the random process was more significant [82]. This is consistent with our findings.

4.3. Potential Functional Traits of Bacteria in Plastisphere

The functions of the microbial community were shown to vary greatly between the soil and plastisphere (PE and PLA) (Figure 7). The predicted abundance of some metabolic pathways in the plastisphere increased (Figure 9). It is particularly noteworthy that the metabolic processes of infectious diseases and drug resistance were promoted in the PLA plastisphere, which indicates that a greater metabolic potential was possessed by the PLA plastisphere [53]. Previous studies have pointed out that the plastisphere is more resistant to antibiotics and serves as a hot spot for acquiring and spreading antibiotic resistance [83]. In contrast, the metabolic level of the PE plastisphere is relatively low. Another study found that the PLA plastisphere had more potential pathogens observed than the PE plastisphere [84], which aligns with our present research findings. In addition, we also focused on the investigation of the functional groups related to pathogenicity, mainly considering its direct ecological risk to the agroecosystem. Based on FAPROTAX analysis (Figure 8), in the PLA plastisphere, the metabolic pathways related to degradation, plant pathogens, carbon, nitrogen, and sulfur were significantly enhanced. These functional differences are likely to be directly related to the different degradation mechanisms of substrates and the enrichment characteristics of specific degradation bacterial taxa [85]. Carbon sources from PLA MPs during the degradation process can be used by microorganisms [86,87,88], thereby increasing the abundance of metabolic functions of microorganisms. In this way, the PLA plastisphere can accommodate more microorganisms that can mediate these metabolic pathways to obtain energy, support their own activities, and influence the biogeochemical cycle of soil [89,90]. According to previous studies, as an important agricultural plant pathogen, Pseudomonas syringe is rich in approximately 60 different pathogenic variants [91]. These pathogenic variants can infect a variety of monocotyledonous and dicotyledonous crops [92]. Another study has demonstrated that high concentrations of PLA MPs (10%) significantly impact legume growth, resulting in reduced maize leaf biomass and chlorophyll content compared with conventional MPs [93]. It not only affects crop yield and quality but also increases the cost of control, causing substantial economic losses to agricultural production [94]. A further study has indicated that PLA MPs can induce more severe effects on organisms, including increased oxidative stress, compromised antioxidant defenses, and neurotoxicity [58]. In view of the degradation cycle of PLA MPs in soil, we can infer that PLA MPs may bring more serious negative effects and greater ecological risks to agriculture in a short time [95,96]. These indicate that compared with conventional MPs, biodegradable MPs may increase the number of potential pathogens, participate in a variety of ecological processes, and pose a higher potential risk to soil ecosystem health.

5. Conclusions

This study systematically revealed differential structural, co-occurrence networks, and functional changes in bacterial communities within soil and the plastisphere (PE and PLA) across different land use types in situ. The plastisphere (PE and PLA) created a unique microbial habitat, where the diversity of bacterial communities and the complexity of co-occurrence network were significantly lower than those in soil environments, and random processes dominated bacterial community assembly. In terms of microbial function, the plastisphere showed higher enrichment in metabolic pathways related to pathogenicity, plastic degradation, carbon, nitrogen, and sulfur cycling than soil. The bacterial communities in the PLA plastisphere exhibited a marked increase in metabolic potential related to drug resistance and infectious diseases. In conclusion, the environmental context shaped by different land use types is a key factor regulating changes in the diversity and structure of bacterial communities in short-term studies. In contrast, the plastic types themselves did not vary much. Compared with conventional MPs, biodegradable MPs may pose a greater risk to soil health. Future research should not only focus on the long-term ecological effects of plastic pollution and its impact on the biogeochemical cycle but also explore the influence of different MP–soil interaction scenarios. For instance, studies could be designed to homogenize MP particles within soil samples and then recover them for analysis. This may help to clarify whether the distinct bacterial community characteristics observed in the plastisphere in our current study would persist or change, considering the potential confounding effects of MPs spatial distribution in the soil matrix.

Supplementary Materials

The following supporting information can be downloaded at www.mdpi.com/article/10.3390/agriculture15070778/s1, Table S1. Physical and chemical properties of soil. Table S2. The topological characteristics of networks. Figure S1. The location of the study area is depicted via satellite imagery (Site 1, Site 2, Site 3 and Site 4). Figure S2. EDS Spectroscopy of GB (a,d,g,j), PE (b,e,h,k) and PLA(c,f,i,l) MPs under different land use types. Figure S3. Fourier transform infrared spectroscopy (FTIR) of (a) GB, (b) PE, (c) PLA and native MPs (CK) under different treatments. Figure S4. Venn diagram shows the number of shared bacterial ASVs in GB, plastisphere (PE and PLA) and soil. Figure S5. The relative abundance of different family (top 10) in soil, GB and plastisphere (PE and PLA).

Author Contributions

Writing−original draft, Y.W.; visualization, Y.W.; methodology, Y.W., H.W. and J.Z.; investigation, Y.W., Z.Z., S.Z., W.Z., Z.S. and Z.L.; data curation, Y.W., Z.Z., S.Z., W.Z., Z.S. and Z.L.; writing—review and editing, H.W. and J.Z.; supervision, J.Z.; project administration, H.W. and J.Z.; funding acquisition, J.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Natural Science Foundation of China (U1701236 and 32471637), the Laboratory of Lingnan Modern Agriculture Project (NT2021010), and the Guangdong Provincial Program of Science and Technology (2019B030301007).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Rodrigues, M.O.; Abrantes, N.; Gonçalves, F.; Nogueira, H.; Marques, J.C.; Gonçalves, A.M. Impacts of plastic products used in daily life on the environment and human health: What is known? Environ. Toxicol. Pharmacol. 2019, 72, 103239. [Google Scholar] [CrossRef]
  2. Kumar, M.; Xiong, X.; He, M.; Tsang, D.C.; Gupta, J.; Khan, E.; Harrad, S.; Hou, D.; Ok, Y.S.; Bolan, N.S. Microplastics as pollutants in agricultural soils. Environ. Pollut. 2020, 265, 114980. [Google Scholar] [CrossRef] [PubMed]
  3. Surendran, U.; Jayakumar, M.; Raja, P.; Gopinath, G.; Chellam, P.V. Microplastics in terrestrial ecosystem: Sources and migration in soil environment. Chemosphere 2023, 318, 137946. [Google Scholar] [CrossRef] [PubMed]
  4. Kumar, V.; Singh, E.; Singh, S.; Pandey, A.; Bhargava, P.C. Micro-and nano-plastics (MNPs) as emerging pollutant in ground water: Environmental impact, potential risks, limitations and way forward towards sustainable management. Chem. Eng. J. 2023, 459, 141568. [Google Scholar] [CrossRef]
  5. Sorasan, C.; Edo, C.; González-Pleiter, M.; Fernández-Piñas, F.; Leganés, F.; Rodríguez, A.; Rosal, R. Ageing and fragmentation of marine microplastics. Sci. Total Environ. 2022, 827, 154438. [Google Scholar] [CrossRef] [PubMed]
  6. Dimassi, S.N.; Hahladakis, J.N.; Yahia, M.N.D.; Ahmad, M.I.; Sayadi, S.; Al-Ghouti, M.A. Degradation-fragmentation of marine plastic waste and their environmental implications: A critical review. Arab. J. Chem. 2022, 15, 104262. [Google Scholar] [CrossRef]
  7. Shah, A.A.; Hasan, F.; Hameed, A.; Ahmed, S. Biological degradation of plastics: A comprehensive review. Biotechnol. Adv. 2008, 26, 246–265. [Google Scholar] [CrossRef]
  8. Wang, J.; Liu, X.; Li, Y.; Powell, T.; Wang, X.; Wang, G.; Zhang, P. Microplastics as contaminants in the soil environment: A mini-review. Sci. Total Environ. 2019, 691, 848–857. [Google Scholar] [CrossRef]
  9. Elizalde-Velázquez, G.A.; Gómez-Oliván, L.M. Microplastics in aquatic environments: A review on occurrence, distribution, toxic effects, and implications for human health. Sci. Total Environ. 2021, 780, 146551. [Google Scholar] [CrossRef]
  10. Hou, J.; Xu, X.; Yu, H.; Xi, B.; Tan, W. Comparing the long-term responses of soil microbial structures and diversities to polyethylene microplastics in different aggregate fractions. Environ. Int. 2021, 149, 106398. [Google Scholar] [CrossRef]
  11. Wu, C.; Ma, Y.; Wang, D.; Shan, Y.; Song, X.; Hu, H.; Ren, X.; Ma, X.; Cui, J.; Ma, Y. Integrated microbiology and metabolomics analysis reveal plastic mulch film residue affects soil microorganisms and their metabolic functions. J. Hazard. Mater. 2022, 423, 127258. [Google Scholar] [CrossRef] [PubMed]
  12. Zhu, M.; Qi, X.; Yuan, Y.; Zhou, H.; Rong, X.; Dang, Z.; Yin, H. Deciphering the distinct successional patterns and potential roles of abundant and rare microbial taxa of urban riverine plastisphere. J. Hazard. Mater. 2023, 450, 131080. [Google Scholar] [CrossRef] [PubMed]
  13. Dong, H.; Chen, Y.; Wang, J.; Zhang, Y.; Zhang, P.; Li, X.; Zou, J.; Zhou, A. Interactions of microplastics and antibiotic resistance genes and their effects on the aquaculture environments. J. Hazard. Mater. 2021, 403, 123961. [Google Scholar] [CrossRef] [PubMed]
  14. Syranidou, E.; Kalogerakis, N. Interactions of microplastics, antibiotics and antibiotic resistant genes within WWTPs. Sci. Total Environ. 2022, 804, 150141. [Google Scholar] [CrossRef]
  15. Zhu, D.; Ma, J.; Li, G.; Rillig, M.C.; Zhu, Y. Soil plastispheres as hotspots of antibiotic resistance genes and potential pathogens. ISME J. 2022, 16, 521–532. [Google Scholar] [CrossRef]
  16. Torres, F.G.; Dioses-Salinas, D.C.; Pizarro-Ortega, C.I.; De-la-Torre, G.E. Sorption of chemical contaminants on degradable and non-degradable microplastics: Recent progress and research trends. Sci. Total Environ. 2021, 757, 143875. [Google Scholar] [CrossRef]
  17. Liu, L.; Xu, M.; Ye, Y.; Zhang, B. On the degradation of (micro) plastics: Degradation methods, influencing factors, environmental impacts. Sci. Total Environ. 2022, 806, 151312. [Google Scholar] [CrossRef]
  18. Miri, S.; Saini, R.; Davoodi, S.M.; Pulicharla, R.; Brar, S.K.; Magdouli, S. Biodegradation of microplastics: Better late than never. Chemosphere 2022, 286, 131670. [Google Scholar] [CrossRef]
  19. Agarwal, S. Biodegradable polymers: Present opportunities and challenges in providing a microplastic-free environment. Macromol. Chem. Phys. 2020, 221, 2000017. [Google Scholar] [CrossRef]
  20. Yuan, J.; Ma, J.; Sun, Y.; Zhou, T.; Zhao, Y.; Yu, F. Microbial degradation and other environmental aspects of microplastics/plastics. Sci. Total Environ. 2020, 715, 136968. [Google Scholar] [CrossRef]
  21. Cai, Z.; Li, M.; Zhu, Z.; Wang, X.; Huang, Y.; Li, T.; Gong, H.; Yan, M. Biological degradation of plastics and microplastics: A recent perspective on associated mechanisms and influencing factors. Microorganisms 2023, 11, 1661. [Google Scholar] [CrossRef] [PubMed]
  22. Zettler, E.R.; Mincer, T.J.; Amaral-Zettler, L.A. Life in the “plastisphere”: Microbial communities on plastic marine debris. Environ. Sci. Technol. 2013, 47, 7137–7146. [Google Scholar] [CrossRef] [PubMed]
  23. Ya, H.; Xing, Y.; Zhang, T.; Lv, M.; Jiang, B. LDPE microplastics affect soil microbial community and form a unique plastisphere on microplastics. Appl. Soil Ecol. 2022, 180, 104623. [Google Scholar] [CrossRef]
  24. Wang, C.; Wang, L.; Ok, Y.S.; Tsang, D.C.; Hou, D. Soil plastisphere: Exploration methods, influencing factors, and ecological insights. J. Hazard. Mater. 2022, 430, 128503. [Google Scholar] [CrossRef]
  25. Sun, Y.; Shi, J.; Wang, X.; Ding, C.; Wang, J. Deciphering the mechanisms shaping the plastisphere microbiota in soil. Msystems 2022, 7, e322–e352. [Google Scholar] [CrossRef]
  26. Zhai, X.; Zhang, X.; Yu, M. Microbial colonization and degradation of marine microplastics in the plastisphere: A review. Front. Microbiol. 2023, 14, 1127308. [Google Scholar] [CrossRef]
  27. Cao, Y.; Zhao, M.; Ma, X.; Song, Y.; Zuo, S.; Li, H.; Deng, W. A critical review on the interactions of microplastics with heavy metals: Mechanism and their combined effect on organisms and humans. Sci. Total Environ. 2021, 788, 147620. [Google Scholar] [CrossRef]
  28. Kim, J.; Yu, Y.; Choi, J. Toxic effects on bioaccumulation, hematological parameters, oxidative stress, immune responses and neurotoxicity in fish exposed to microplastics: A review. J. Hazard. Mater. 2021, 413, 125423. [Google Scholar] [CrossRef]
  29. Yu, H.; Zhang, Y.; Tan, W. The “neighbor avoidance effect” of microplastics on bacterial and fungal diversity and communities in different soil horizons. Environ. Sci. Ecotechnol. 2021, 8, 100121. [Google Scholar] [CrossRef]
  30. Alimi, O.S.; Claveau-Mallet, D.; Kurusu, R.S.; Lapointe, M.; Bayen, S.; Tufenkji, N. Weathering pathways and protocols for environmentally relevant microplastics and nanoplastics: What are we missing? J. Hazard. Mater. 2022, 423, 126955. [Google Scholar] [CrossRef]
  31. Xu, X.; Wang, S.; Gao, F.; Li, J.; Zheng, L.; Sun, C.; He, C.; Wang, Z.; Qu, L. Marine microplastic-associated bacterial community succession in response to geography, exposure time, and plastic type in China’s coastal seawaters. Mar. Pollut. Bull. 2019, 145, 278–286. [Google Scholar] [CrossRef] [PubMed]
  32. Zhang, Q.; Wu, J.; Yang, F.; Lei, Y.; Zhang, Q.; Cheng, X. Alterations in soil microbial community composition and biomass following agricultural land use change. Sci. Rep. 2016, 6, 36587. [Google Scholar] [CrossRef] [PubMed]
  33. Wang, H.; Marshall, C.W.; Cheng, M.; Xu, H.; Li, H.; Yang, X.; Zheng, T. Changes in land use driven by urbanization impact nitrogen cycling and the microbial community composition in soils. Sci. Rep. 2017, 7, 44049. [Google Scholar] [CrossRef] [PubMed]
  34. Zhang, X.; Zhang, Y.; Wu, N.; Li, W.; Song, X.; Ma, Y.; Niu, Z. Colonization characteristics of bacterial communities on plastic debris: The localization of immigrant bacterial communities. Water Res. 2021, 193, 116883. [Google Scholar] [CrossRef]
  35. Forero-López, A.D.; Brugnoni, L.I.; Abasto, B.; Rimondino, G.N.; Lassalle, V.L.; Ardusso, M.G.; Nazzarro, M.S.; Martinez, A.M.; Spetter, C.V.; Biancalana, F. Plastisphere on microplastics: In situ assays in an estuarine environment. J. Hazard. Mater. 2022, 440, 129737. [Google Scholar] [CrossRef]
  36. Zhang, M.; Zhao, Y.; Qin, X.; Jia, W.; Chai, L.; Huang, M.; Huang, Y. Microplastics from mulching film is a distinct habitat for bacteria in farmland soil. Sci. Total Environ. 2019, 688, 470–478. [Google Scholar]
  37. Jones, D.L.; Willett, V.B. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol. Biochem. 2006, 38, 991–999. [Google Scholar] [CrossRef]
  38. Brookes, P.C.; Landman, A.; Pruden, G.; Jenkinson, D.S. Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 1985, 17, 837–842. [Google Scholar] [CrossRef]
  39. Roig, B.; Gonzalez, C.; Thomas, O. Simple UV/UV-visible method for nitrogen and phosphorus measurement in wastewater. Talanta 1999, 50, 751–758. [Google Scholar] [CrossRef]
  40. Guo, Y.; Liu, C.; Ye, R.; Duan, Q. Advances on water quality detection by uv-vis spectroscopy. Appl. Sci. 2020, 10, 6874. [Google Scholar] [CrossRef]
  41. Csardi, G.; Nepusz, T. The igraph software package for complex network research. InterJournal Complex Syst. 2006, 2006, 1695. [Google Scholar]
  42. Newman, M.E. Modularity and community structure in networks. Proc. Natl. Acad. Sci. USA 2006, 103, 8577–8582. [Google Scholar] [CrossRef] [PubMed]
  43. Dufrêne, M.; Legendre, P. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol. Monogr. 1997, 67, 345–366. [Google Scholar] [CrossRef]
  44. Ning, D.; Yuan, M.; Wu, L.; Zhang, Y.; Guo, X.; Zhou, X.; Yang, Y.; Arkin, A.P.; Firestone, M.K.; Zhou, J. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nat. Commun. 2020, 11, 4717. [Google Scholar] [CrossRef]
  45. Li, N.; Qu, J.; Yang, J. Microplastics distribution and microbial community characteristics of farmland soil under different mulch methods. J. Hazard. Mater. 2023, 445, 130408. [Google Scholar] [CrossRef]
  46. Feng, X.; Wang, Q.; Sun, Y.; Zhang, S.; Wang, F. Microplastics change soil properties, heavy metal availability and bacterial community in a Pb-Zn-contaminated soil. J. Hazard. Mater. 2022, 424, 127364. [Google Scholar] [CrossRef]
  47. Liu, G.; Bai, Z.; Cui, G.; He, W.; Kong, Z.; Ji, G.; Gong, H.; Li, D. Effects of land use on the soil microbial community in the Songnen Grassland of Northeast China. Front. Microbiol. 2022, 13, 865184. [Google Scholar] [CrossRef]
  48. Sun, Y.; Luo, C.; Jiang, L.; Song, M.; Zhang, D.; Li, J.; Li, Y.; Ostle, N.J.; Zhang, G. Land-use changes alter soil bacterial composition and diversity in tropical forest soil in China. Sci. Total Environ. 2020, 712, 136526. [Google Scholar] [CrossRef]
  49. Gupta, A.; Singh, U.B.; Sahu, P.K.; Paul, S.; Kumar, A.; Malviya, D.; Singh, S.; Kuppusamy, P.; Singh, P.; Paul, D. Linking soil microbial diversity to modern agriculture practices: A review. Int. J. Environ. Res. Public Health 2022, 19, 3141. [Google Scholar] [CrossRef]
  50. Hartmann, M.; Six, J. Soil structure and microbiome functions in agroecosystems. Nat. Rev. Earth Environ. 2023, 4, 4–18. [Google Scholar] [CrossRef]
  51. Li, C.; Wang, L.; Ji, S.; Chang, M.; Wang, L.; Gan, Y.; Liu, J. The ecology of the plastisphere: Microbial composition, function, assembly, and network in the freshwater and seawater ecosystems. Water Res. 2021, 202, 117428. [Google Scholar] [CrossRef] [PubMed]
  52. Zhang, S.; Zeng, Y.; Zhu, J.; Cai, Z.; Zhou, J. The structure and assembly mechanisms of plastisphere microbial community in natural marine environment. J. Hazard. Mater. 2022, 421, 126780. [Google Scholar] [CrossRef] [PubMed]
  53. Li, K.; Jia, W.; Xu, L.; Zhang, M.; Huang, Y. The plastisphere of biodegradable and conventional microplastics from residues exhibit distinct microbial structure, network and function in plastic-mulching farmland. J. Hazard. Mater. 2023, 442, 130011. [Google Scholar] [CrossRef] [PubMed]
  54. Huang, Y.; Zhao, Y.; Wang, J.; Zhang, M.; Jia, W.; Qin, X. LDPE microplastic films alter microbial community composition and enzymatic activities in soil. Environ. Pollut. 2019, 254, 112983. [Google Scholar] [CrossRef]
  55. Feng, S.; Wang, H.; Wang, Y.; Cheng, Q. A review of the occurrence and degradation of biodegradable microplastics in soil environments. Sci. Total Environ. 2023, 904, 166855. [Google Scholar] [CrossRef]
  56. Bao, R.; Fu, D.; Fan, Z.; Peng, X.; Peng, L. Aging of microplastics and their role as vector for copper in aqueous solution. Gondwana Res. 2022, 108, 81–90. [Google Scholar] [CrossRef]
  57. Yu, H.; Zhang, Y.; Tan, W.; Zhang, Z. Microplastics as an emerging environmental pollutant in agricultural soils: Effects on ecosystems and human health. Front. Environ. Sci. 2022, 10, 855292. [Google Scholar] [CrossRef]
  58. Ainali, N.M.; Kalaronis, D.; Evgenidou, E.; Kyzas, G.Z.; Bobori, D.C.; Kaloyianni, M.; Yang, X.; Bikiaris, D.N.; Lambropoulou, D.A. Do poly (lactic acid) microplastics instigate a threat? A perception for their dynamic towards environmental pollution and toxicity. Sci. Total Environ. 2022, 832, 155014. [Google Scholar] [CrossRef]
  59. Chen, J.; Wu, J.; Sherrell, P.C.; Chen, J.; Wang, H.; Zhang, W.X.; Yang, J. How to build a microplastics-free environment: Strategies for microplastics degradation and plastics recycling. Adv. Sci. 2022, 9, 2103764. [Google Scholar] [CrossRef]
  60. Zhang, X.; Li, Y.; Ouyang, D.; Lei, J.; Tan, Q.; Xie, L.; Li, Z.; Liu, T.; Xiao, Y.; Farooq, T.H. Systematical review of interactions between microplastics and microorganisms in the soil environment. J. Hazard. Mater. 2021, 418, 126288. [Google Scholar] [CrossRef]
  61. An, Q.; Zheng, N.; Pan, J.; Ji, Y.; Wang, S.; Li, X.; Chen, C.; Peng, L.; Wang, B. Association between plant microbiota and cadmium uptake under the influence of microplastics with different particle sizes. Environ. Int. 2024, 190, 108938. [Google Scholar] [CrossRef] [PubMed]
  62. Rong, L.; Zhao, L.; Zhao, L.; Cheng, Z.; Yao, Y.; Yuan, C.; Wang, L.; Sun, H. LDPE microplastics affect soil microbial communities and nitrogen cycling. Sci. Total Environ. 2021, 773, 145640. [Google Scholar] [CrossRef]
  63. Dey, S.; Rout, A.K.; Behera, B.K.; Ghosh, K. Plastisphere community assemblage of aquatic environment: Plastic-microbe interaction, role in degradation and characterization technologies. Environ. Microbiome 2022, 17, 32. [Google Scholar] [CrossRef] [PubMed]
  64. Wilkes, R.; Aristilde, L. Degradation and metabolism of synthetic plastics and associated products by Pseudomonas sp.: Capabilities and challenges. J. Appl. Microbiol. 2017, 123, 582–593. [Google Scholar] [CrossRef] [PubMed]
  65. Tu, C.; Liu, Y.; Li, L.; Li, Y.; Vogts, A.; Luo, Y.; Waniek, J.J. Structural and functional characteristics of microplastic associated biofilms in response to temporal dynamics and polymer types. Bull. Environ. Contam. Toxicol. 2021, 107, 633–639. [Google Scholar] [CrossRef]
  66. Wang, P.; Liu, J.; Han, S.; Wang, Y.; Duan, Y.; Liu, T.; Hou, L.; Zhang, Z.; Li, L.; Lin, Y. Polyethylene mulching film degrading bacteria within the plastisphere: Co-culture of plastic degrading strains screened by bacterial community succession. J. Hazard. Mater. 2023, 442, 130045. [Google Scholar] [CrossRef]
  67. Cui, B.; Fu, S.; Hao, X.; Zhou, D. Synergistic effects of simultaneous coupling ozonation and biodegradation for coking wastewater treatment: Advances in COD removal, toxic elimination, and microbial regulation. Chemosphere 2023, 318, 137956. [Google Scholar] [CrossRef]
  68. Luo, J.; Banerjee, S.; Ma, Q.; Liao, G.; Hu, B.; Zhao, H.; Li, T. Organic fertilization drives shifts in microbiome complexity and keystone taxa increase the resistance of microbial mediated functions to biodiversity loss. Biol. Fertil. Soils 2023, 59, 441–458. [Google Scholar] [CrossRef]
  69. Sun, Y.; Wang, X.; Xia, S.; Zhao, J. Cu (II) adsorption on poly (lactic acid) microplastics: Significance of microbial colonization and degradation. Chem. Eng. J. 2022, 429, 132306. [Google Scholar] [CrossRef]
  70. Mishra, S.; Swain, S.; Sahoo, M.; Mishra, S.; Das, A.P. Microbial colonization and degradation of microplastics in aquatic ecosystem: A review. Geomicrobiol. J. 2022, 39, 259–269. [Google Scholar] [CrossRef]
  71. Sun, X.; Xiang, H.; Xiong, H.; Fang, Y.; Wang, Y. Bioremediation of microplastics in freshwater environments: A systematic review of biofilm culture, degradation mechanisms, and analytical methods. Sci. Total Environ. 2023, 863, 160953. [Google Scholar] [CrossRef] [PubMed]
  72. Qiu, L.; Zhang, Q.; Zhu, H.; Reich, P.B.; Banerjee, S.; van der Heijden, M.G.; Sadowsky, M.J.; Ishii, S.; Jia, X.; Shao, M. Erosion reduces soil microbial diversity, network complexity and multifunctionality. ISME J. 2021, 15, 2474–2489. [Google Scholar] [CrossRef] [PubMed]
  73. Wan, X.; Gao, Q.; Zhao, J.; Feng, J.; van Nostrand, J.D.; Yang, Y.; Zhou, J. Biogeographic patterns of microbial association networks in paddy soil within Eastern China. Soil Biol. Biochem. 2020, 142, 107696. [Google Scholar] [CrossRef]
  74. Sun, Y.; Li, X.; Cao, N.; Duan, C.; Ding, C.; Huang, Y.; Wang, J. Biodegradable microplastics enhance soil microbial network complexity and ecological stochasticity. J. Hazard. Mater. 2022, 439, 129610. [Google Scholar] [CrossRef]
  75. Fan, P.; Yu, H.; Xi, B.; Tan, W. A review on the occurrence and influence of biodegradable microplastics in soil ecosystems: Are biodegradable plastics substitute or threat? Environ. Int. 2022, 163, 107244. [Google Scholar] [CrossRef]
  76. Liu, N.; Hu, H.; Ma, W.; Deng, Y.; Wang, Q.; Luo, A.; Meng, J.; Feng, X.; Wang, Z. Relative importance of deterministic and stochastic processes on soil microbial community assembly in temperate grasslands. Microorganisms 2021, 9, 1929. [Google Scholar] [CrossRef]
  77. Bissett, A.; Brown, M.V.; Siciliano, S.D.; Thrall, P.H. Microbial community responses to anthropogenically induced environmental change: Towards a systems approach. Ecol. Lett. 2013, 16, 128–139. [Google Scholar] [CrossRef]
  78. Zhou, J.; Ning, D. Stochastic community assembly: Does it matter in microbial ecology? Microbiol. Mol. Biol. Rev. 2017, 81, 10–1128. [Google Scholar] [CrossRef]
  79. Graham, E.B.; Stegen, J.C. Dispersal-based microbial community assembly decreases biogeochemical function. Processes 2017, 5, 65. [Google Scholar] [CrossRef]
  80. Caruso, T.; Chan, Y.; Lacap, D.C.; Lau, M.C.; McKay, C.P.; Pointing, S.B. Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J. 2011, 5, 1406–1413. [Google Scholar] [CrossRef]
  81. Purahong, W.; Wahdan, S.F.M.; Heinz, D.; Jariyavidyanont, K.; Sungkapreecha, C.; Tanunchai, B.; Sansupa, C.; Sadubsarn, D.; Alaneed, R.; Heintz-Buschart, A. Back to the future: Decomposability of a biobased and biodegradable plastic in field soil environments and its microbiome under ambient and future climates. Environ. Sci. Technol. 2021, 55, 12337–12351. [Google Scholar] [CrossRef] [PubMed]
  82. Li, W.; Xiao, Y. Microplastics increase soil microbial network complexity and trigger diversity-driven community assembly. Environ. Pollut. 2023, 333, 122095. [Google Scholar] [CrossRef] [PubMed]
  83. Yang, K.; Chen, Q.; Chen, M.; Li, H.; Liao, H.; Pu, Q.; Zhu, Y.; Cui, L. Temporal dynamics of antibiotic resistome in the plastisphere during microbial colonization. Environ. Sci. Technol. 2020, 54, 11322–11332. [Google Scholar] [CrossRef] [PubMed]
  84. Li, K.; Xu, L.; Bai, X.; Zhang, G.; Zhang, M.; Huang, Y. Potential environmental risks of field bio/non-degradable microplastic from mulching residues in farmland: Evidence from metagenomic analysis of plastisphere. J. Hazard. Mater. 2024, 465, 133428. [Google Scholar] [CrossRef]
  85. Yao, Y.; Wang, L.; Pan, S.; Li, G.; Liu, H.; Xiu, W.; Gong, L.; Zhao, J.; Zhang, G.; Yang, D. Can microplastics mediate soil properties, plant growth and carbon/nitrogen turnover in the terrestrial ecosystem? Ecosyst. Health Sustain. 2022, 8, 2133638. [Google Scholar] [CrossRef]
  86. Bhardwaj, H.; Gupta, R.; Tiwari, A. Communities of microbial enzymes associated with biodegradation of plastics. J. Polym. Environ. 2013, 21, 575–579. [Google Scholar] [CrossRef]
  87. Zhang, H.; Huang, Y.; Shen, J.; Xu, F.; Hou, H.; Xie, C.; Wang, B.; An, S. Mechanism of polyethylene and biodegradable microplastic aging effects on soil organic carbon fractions in different land-use types. Sci. Total Environ. 2024, 912, 168961. [Google Scholar] [CrossRef]
  88. Wang, Q.; Feng, X.; Liu, Y.; Cui, W.; Sun, Y.; Zhang, S.; Wang, F. Effects of microplastics and carbon nanotubes on soil geochemical properties and bacterial communities. J. Hazard. Mater. 2022, 433, 128826. [Google Scholar] [CrossRef]
  89. Shi, J.; Wang, Z.; Peng, Y.; Zhang, Z.; Fan, Z.; Wang, J.; Wang, X. Microbes drive metabolism, community diversity, and interactions in response to microplastic-induced nutrient imbalance. Sci. Total Environ. 2023, 877, 162885. [Google Scholar] [CrossRef]
  90. Chen, H.; Wang, Y.; Sun, X.; Peng, Y.; Xiao, L. Mixing effect of polylactic acid microplastic and straw residue on soil property and ecological function. Chemosphere 2020, 243, 125271. [Google Scholar] [CrossRef]
  91. Hirano, S.S.; Upper, C.D. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—A pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 2000, 64, 624–653. [Google Scholar] [CrossRef] [PubMed]
  92. Lipps, S.M.; Samac, D.A. Pseudomonas viridiflava: An internal outsider of the Pseudomonas syringae species complex. Mol. Plant Pathol. 2022, 23, 3–15. [Google Scholar] [CrossRef] [PubMed]
  93. Wang, F.; Zhang, X.; Zhang, S.; Zhang, S.; Sun, Y. Interactions of microplastics and cadmium on plant growth and arbuscular mycorrhizal fungal communities in an agricultural soil. Chemosphere 2020, 254, 126791. [Google Scholar] [CrossRef] [PubMed]
  94. Córdova, P.; Rivera-González, J.P.; Rojas-Martínez, V.; Fiore, N.; Bastías, R.; Zamorano, A.; Vera, F.; Barrueto, J.; Díaz, B.; Ilabaca-Díaz, C. Phytopathogenic Pseudomonas syringae as a threat to agriculture: Perspectives of a promising biological control using bacteriophages and microorganisms. Horticulturae 2023, 9, 712. [Google Scholar] [CrossRef]
  95. Liu, R.; Liang, J.; Yang, Y.; Jiang, H.; Tian, X. Effect of polylactic acid microplastics on soil properties, soil microbials and plant growth. Chemosphere 2023, 329, 138504. [Google Scholar] [CrossRef]
  96. Serrano-Ruiz, H.; Martin-Closas, L.; Pelacho, A.M. Biodegradable plastic mulches: Impact on the agricultural biotic environment. Sci. Total Environ. 2021, 750, 141228. [Google Scholar] [CrossRef]
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Figure 1. Surface morphology analysis of GBs (a) and MPs (b,c) was conducted. Scanning electron microscope (SEM) micrographs of GB, PE, and PLA MPs, together with pristine GBs and MPs as the control (CK), having been buried for 2 months, were analyzed. The analysis was carried out in vegetable fields (VF), orchards (OR), paddy fields (PF), and woodlands (WL).
Figure 1. Surface morphology analysis of GBs (a) and MPs (b,c) was conducted. Scanning electron microscope (SEM) micrographs of GB, PE, and PLA MPs, together with pristine GBs and MPs as the control (CK), having been buried for 2 months, were analyzed. The analysis was carried out in vegetable fields (VF), orchards (OR), paddy fields (PF), and woodlands (WL).
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Figure 2. The bacterial community structure in soil, GBs, and the plastisphere (PE and PLA) was analyzed. (a) Shannon index; (b) Faith’s PD index of bacterial communities in soil, GBs, and the plastisphere (PE and PLA); (c) PCoA plots visualizing the difference between the soil, GBs, and different plastisphere-treated groups. The percentages in brackets show the percentage of variation explained by those principal components; (d) Bray–Curtis dissimilarity of bacterial community structures in soil, GBs, and the plastisphere (PE and PLA). Different uppercase letters indicate significant differences between soil, GBs, and the plastisphere (PE and PLA) across different land use types, while lowercase letters denote significant differences within the same land use type across different treatments. For two-way ANOVA, p values with an asterisk indicate statistical significance (p < 0.05). VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 2. The bacterial community structure in soil, GBs, and the plastisphere (PE and PLA) was analyzed. (a) Shannon index; (b) Faith’s PD index of bacterial communities in soil, GBs, and the plastisphere (PE and PLA); (c) PCoA plots visualizing the difference between the soil, GBs, and different plastisphere-treated groups. The percentages in brackets show the percentage of variation explained by those principal components; (d) Bray–Curtis dissimilarity of bacterial community structures in soil, GBs, and the plastisphere (PE and PLA). Different uppercase letters indicate significant differences between soil, GBs, and the plastisphere (PE and PLA) across different land use types, while lowercase letters denote significant differences within the same land use type across different treatments. For two-way ANOVA, p values with an asterisk indicate statistical significance (p < 0.05). VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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Figure 3. The phylum composition of bacterial communities in GBs, the plastisphere (PE and PLA), and soil samples was analyzed. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 3. The phylum composition of bacterial communities in GBs, the plastisphere (PE and PLA), and soil samples was analyzed. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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Figure 4. (a,b,e,f) The distribution of ASVs in each treatment sample across different land uses is shown in the SPEC-OCCU plot. ASVs with both specificity and occupancy values greater than or equal to 0.7 are selected, with the x-axis representing occupancy and the y-axis representing specificity. The size and color of each ASVs indicate its relative abundance and bacterial phylum, respectively. (c,d,g,h) The number of specific ASVs (specialists) in each land use treatment is presented. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 4. (a,b,e,f) The distribution of ASVs in each treatment sample across different land uses is shown in the SPEC-OCCU plot. ASVs with both specificity and occupancy values greater than or equal to 0.7 are selected, with the x-axis representing occupancy and the y-axis representing specificity. The size and color of each ASVs indicate its relative abundance and bacterial phylum, respectively. (c,d,g,h) The number of specific ASVs (specialists) in each land use treatment is presented. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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Figure 5. Biotic co-occurrence network and topological parameters of bacterial communities in soil, GBs, and the plastisphere (PE and PLA). Different modules are presented in various colors. (a) VF denotes vegetable fields, (b) OR denotes orchards, (c) PF denotes paddy fields, and (d) WL denotes woodlands.
Figure 5. Biotic co-occurrence network and topological parameters of bacterial communities in soil, GBs, and the plastisphere (PE and PLA). Different modules are presented in various colors. (a) VF denotes vegetable fields, (b) OR denotes orchards, (c) PF denotes paddy fields, and (d) WL denotes woodlands.
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Figure 6. (a–d) The mechanisms of bacterial community assembly were examined, and the proportions of different ecological processes were analyzed. (e) Changes in the five ecological processes across plastisphere treatments were observed. Abbreviations: Homogeneous selection (HoS), heterogeneous selection (HeS), dispersal limitation (DL), homogenizing dispersal (HD), and drift (DR). VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 6. (a–d) The mechanisms of bacterial community assembly were examined, and the proportions of different ecological processes were analyzed. (e) Changes in the five ecological processes across plastisphere treatments were observed. Abbreviations: Homogeneous selection (HoS), heterogeneous selection (HeS), dispersal limitation (DL), homogenizing dispersal (HD), and drift (DR). VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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Figure 7. KEGG function prediction based on the 16S rRNA sequence under different land use types. In the figure, high abundance in the corresponding samples is represented by pink, while low abundance is indicated by green. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 7. KEGG function prediction based on the 16S rRNA sequence under different land use types. In the figure, high abundance in the corresponding samples is represented by pink, while low abundance is indicated by green. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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Figure 8. Heat maps based on FAPROTAX showing the main differences in predictive functions under different land uses. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 8. Heat maps based on FAPROTAX showing the main differences in predictive functions under different land uses. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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Figure 9. Schematic representation of MPs multifunctionality changes in different land use types under in situ conditions based on the results of this study. The red arrow represents an increase. The color changes from light to dark as the abundance increases. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
Figure 9. Schematic representation of MPs multifunctionality changes in different land use types under in situ conditions based on the results of this study. The red arrow represents an increase. The color changes from light to dark as the abundance increases. VF denotes vegetable fields, OR denotes orchards, PF denotes paddy fields, and WL denotes woodlands.
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MDPI and ACS Style

Wang, Y.; Zhang, Z.; Zhang, S.; Zhuang, W.; Shi, Z.; Liu, Z.; Wei, H.; Zhang, J. Land Use Rather than Microplastic Type Determines the Diversity and Structure of Plastisphere Bacterial Communities. Agriculture 2025, 15, 778. https://doi.org/10.3390/agriculture15070778

AMA Style

Wang Y, Zhang Z, Zhang S, Zhuang W, Shi Z, Liu Z, Wei H, Zhang J. Land Use Rather than Microplastic Type Determines the Diversity and Structure of Plastisphere Bacterial Communities. Agriculture. 2025; 15(7):778. https://doi.org/10.3390/agriculture15070778

Chicago/Turabian Style

Wang, Yangyang, Zixuan Zhang, Shuang Zhang, Wanlin Zhuang, Zhaoji Shi, Ziqiang Liu, Hui Wei, and Jiaen Zhang. 2025. "Land Use Rather than Microplastic Type Determines the Diversity and Structure of Plastisphere Bacterial Communities" Agriculture 15, no. 7: 778. https://doi.org/10.3390/agriculture15070778

APA Style

Wang, Y., Zhang, Z., Zhang, S., Zhuang, W., Shi, Z., Liu, Z., Wei, H., & Zhang, J. (2025). Land Use Rather than Microplastic Type Determines the Diversity and Structure of Plastisphere Bacterial Communities. Agriculture, 15(7), 778. https://doi.org/10.3390/agriculture15070778

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