Emerging Microplastics Alter the Influences of Soil Animals on the Fungal Community Structure in Determining the Litter Decomposition of a Deciduous Tree

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New environmental contaminants, represented by microplastics, enter forest ecosystems through atmospheric sedimentation, overland runoff, and human activities and interfere with the physiological functions of soil organisms [50,51]. At present, the impact of microplastics on soil animals has mostly been evaluated in terms of ecotoxicology [52]. Exposure to high-density polyethylene microplastics significantly reduces the biomass of earthworms [26]. Moreover, soil microplastics inhibit the movement of springtails [23]. We also reached the conclusion that the addition of microplastics significantly reduces the weight of the earthworms, which showed negative growth in our study (Figure 3a). However, we did not find any effect of HDPE−MPs on springtails, possibly because the microplastics we selected had larger particle sizes and were not swallowed by springtails. Previous research supports our conclusions; by feeding springtails polyethylene microplastics of three different sizes (2, 3, 4, and 66 μm) and using fluorescence microscopy, the edible size of the microplastics was observed to be less than 66.0 ± 10.9 μm in the gut [14]. Therefore, in future studies, we should pay attention to the effects of the type, particle size, and concentration of microplastics on the biochemical cycles of soil decomposers. Studies have shown that MPs can decrease the relative abundance of soil microorganisms and affect the diversity and richness of the microbial community structure [53]. Consistent with our findings, HDPE−MPs decreased the fungal Shannon, Simpson, and Chao1 diversity indices of litter (Figure 1), possibly because microplastics can compete with soil microbes for niches in which microbes can grow and move and reduce the abundance of dominant species; however, our results indicate no significant effects of interactions between MPs and microorganisms on litter fungal diversity (Figure 1). Notably, due to the influence of microplastics on soil animals, the inhibitory effect of soil animals on the microbial decomposition of litter decreased, and the mass loss decreased by 10.8% (Figure 1a; L and LA vs. LH and LHA). Moreover, the Shannon index increased by 9.84% (Figure 1b), the Simpson index increased by 8.84% (Figure 1c), and the Chao 1 index decreased by 4.82% (Figure 1d). However, earlier reports have been mixed; for example, microplastics may affect the feeding activities of soil animals, causing digestive tract damage [13]. This ecotoxicity may affect the bio-decomposition of litter by soil animals, thereby reducing mass loss. This finding contradicts our conclusion and contradicts our second hypothesis. Microplastics affect feeding activities and result in weight loss in earthworms, weakening the regulatory effect of soil animals on microbial community structure. We also found that the relative abundance of Ascomycetes increased by 1.13% and that the abundance of Basidiomycetes decreased by 1.24% after microplastics were added (Figure 4b). However, compared with those in the absence of microplastics, both the increase and decrease in soluble protein levels slowed, which also indicates that the feeding of Basidiomycetes was reduced due to the effect of microplastics on the feeding activities of soil animals. In addition, the reduction in white rot fungi was also lower in the presence of microplastics than in the absence of microplastics (Table 3). We also found that Epicoccum, Hemimycena, and Malassezia were the biomarkers associated with HDPE−MPs treatment and played important roles in litter decomposition (Figure 5). We also found that the Sordariomycetes fungus was differentially expressed in HDPE−MPs treatment and may be resistant to microplastic stress. Recently, results have confirmed that plastic-degrading fungi are found in eleven classes of the fungal phylum Ascomycota. Sordariomycetes also supported our findings [54]. In addition, HDPE−MPs decreased the proportion of soil macroaggregate structures (Figure 2). The strong surface tension of microplastics may increase the accumulation of organic matter and microflora, which affects the stability of soil aggregates [55]. Moreover, the negative charge of microplastics may repel soil particles, reduce the stability of aggregates, and increase the ease with which microorganisms gather on the litter surface [56], thus increasing the decomposition of litter. When microplastics are added, the complexity of the co-occurrence networks decreases (Figure 7; LHA). In conclusion, we can conclude that HDPE−MPs exposure not only altered soil animal activities but also further changed the fungal community and fungal function. In conclusion, our study showed that compared with soil-animal-regulated microbial degradation, HDPE can reduce the inhibition of microbial community complexity and litter decomposition by soil animals. Nevertheless, in our study, only representative soil animals and microplastics were selected for preliminary exploration. Although the influence of new environmental pollutants represented by microplastics on nutrient cycling in forest ecosystems has been revealed, future studies should increase the research on different concentrations, different types of microplastics, and more complex soil animal types. Improving the understanding of the impact of microplastics on the biochemical cycle in the context of global pollution will provide theoretical support.

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