1 Introduction

Microorganisms (bacteria, archaea, fungi, and algae) play a foundational role in the earth’s terrestrial ecosystems, mediating biogeochemical cycles and energy flows through processes such as photosynthesis/respiration, nitrogen fixation, and organic matter decomposition that are critical to life. As xenobiotics in the environment, microplastics (MPs, plastic particles with a size less than 5 mm) and nanoplastics (NPs, plastic particles with a size less than 1 μm or 100 nm), which may be manufactured or result from the breakdown of larger polymers, have become ever-present in the environment (Fig. 1) (Wu et al. 2021). During MPs/NPs long-term retention in terrestrial environments, these contaminants will continuously interact with surrounding microorganisms, forming a unique ecosystem referred to as the “plastisphere”. The term “plastisphere” was originally defined as the life on the plastic material, with a particular focus on the microbial community, including some plastic-degrading microbes (Amaral- Zettler et al. 2020). However, a critical issue is that these anthropogenic contaminants are toxic to some terrestrial microorganisms, and the results of that toxic interaction over time can significantly impact microbial community structure and function, with unknown ramifications for ecosystem health. Importantly, MP/NP exposure is a direct result of anthropogenic activity and therefore, any shift in an environmental microbiome will inherently move the system away from its original state. The significance of those changes, as well as the resilience of the system to return to the “ground state” over time, is largely unknown. Considering the diverse array of MPs/NPs, the broad dose range, and the presence of co-contaminants (e.g., retained organic and elemental pollutants, polymer additives) associated with these materials, their risk calculus to a soil microbiome is incredibly complex.

Fig. 1
figure 1

Exposure route and toxicity of MP and NP to microorganisms within the plastisphere in the terrestrial environment

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2 Critical impact of dose and co-contaminant presence on the MP/NP toxicity and risk evaluation

As emerging contaminants, the mechanisms of MPs/NPs toxicity to terrestrial microorganisms are not completely understood, although a number of reports have demonstrated inhibited reproduction and development (Fei et al. 2020; Ya et al. 2022). For example, Li et al. (2021a,b) investigated the effects of microplastics on soil microbial communities when underwent long-term fertilization process and discovered that MPs fertilization samples showed a lower bacterial community (F = 1.78), fungal community (F = 3.04), and CNP (carbon–nitrogen-phosphorus) cycling-related functional genes profile (F = 3.30) than that of the blank control without MPs’ exposure (bacterial community: F = 22.0; fungal community: F = 14.2; CNP genes profile: F = 9.72) according to the PERMANOVA Test (Fig. 1) (Li et al. 2021a). This indicated that MPs/NPs’ exposure in terrestrial ecosystem are responsible to inhibit the growth of certain soil microbiota and alter the soil microbial community structure (Ya et al. 2022; Zhu et al. 2022). Specifically, in comparison with blank control, MPs treatment could inhibit the growth of Acidobacteria, Plantcomycetes, and Proteobacteria (Li et al. 2021a). The authors speculated that the mechanisms of toxicity included induced excessive reactive oxygen species (ROS) production (e.g., hydroxyl radicals •OH, superoxide anion O2•−, and singlet oxygen 1O2), potentially associated with co-contaminants adsorbed upon the surface of MPs/NPs and the presence of plastic additives.

Regarding the impact of exposure, NPs have been shown to interfere with the mitochondrial metabolism after intracellular uptake, inhibiting the activity of intracellular glutathione, decreasing the ability of mitochondria to expel toxic oxides, and finally inducing cell apoptosis (Li et al. 2021b). In contrast to NP, MP exposure to microbes can induce the damage of microbial cell membrane. This is due to the MPs has relatively large size than NPs and unable to enter into the inner side of the cells. (Fig. 1) (Li et al. 2021b). Regarding the ROS which generation induced by environmentally persistent free radicals (EPFRs) associated cell toxicity, it was reported that 60 d of photo aged tire wear particles produced 1.0 × 1017 spins/g ROS of EPFRs, which decreased cell viability for 27 to 45% and increase oxidative stress response for 46 − 93% and inflammatory factor secretion (Liu et al. 2022). Mechanism related to the cell toxicity of ROS species to organisms are mainly referred to the cytotoxicity, oxidative stress response, and proinflammatory cytokine secretion of macrophages. Sampled as inflammation response, ROS produced by MPs/NPs are able to promote the production of mRNA levels of inflammatory potential, including TNF-α, IL-6 mRNA, and iNOS, interfering the inflammation response for macrophages and gene express (Liu et al. 2022). Since we can conclude that ROS species (e.g., hydroxyl radicals •OH, superoxide anion O2•−, and singlet oxygen 1O2) generated as a consequence of MPs/NPs, particularly aged particles, can also increase in sensitive organelles such as the mitochondria, dysregulating the production-digestion balance of ROS, causing organelle damage, and reducing cellular adenosine triphosphate (ATP) production (Fig. 1) (Wang et al. 2020b). Moreover, ROS species can also directly damage the mitochondria, resulting in intracellular oxidative stress and inflammatory response, as well as compromising cell membrane integrity, activity and survival (Gu et al. 2020; Zou et al. 2020).

A critical issue that must be considered is the MP/NP dose. The foundational principle of toxicology is that the dose makes the poison and MP/NP are no exception. For example, it has been reported that MP/NP toxicity is dose dependent for a number of species, including for endpoints such as developmental impacts, cell viability, inflammatory responses, and immune dysfunction (Zou et al. 2020). Specifically, NP exposure at 1 mg/L NP induced intestinal inflammation to benthic clams (Corbicula fluminea) in comparison with the blank control, whereas the opposite effect was observed at 0.1 mg/L. The authors speculated that there was a saturation of the C. fluminea antioxidant system and an imbalance of the intestinal flora (Li et al. 2021b). These studies highlight the importance of dose when conducting investigations and estimating the risk to sensitive terrestrial receptors such as the soil microbiome. However, available dose ranges to quantitate and evaluate the toxicity of MP and NP on terrestrial animals and cell cultures is fairly unknown, although many efforts have emphasized the dose-dependent MPs/NPs’ toxicity effect to diverse organisms (An et al. 2021; Gonzalezfernandez et al. 2018). Hence, in the future, more attention should be concerned on the dose ranges of MP/NP toxicity and risk to terrestrial organisms (or microorganisms); what is high (toxic) and low (non- or less toxic). It is also worth noting that MP/NPs toxicity and risk profiles in terrestrial systems are markedly different from those in freshwater and marine aquatic ecosystems.

Another critical issue to consider when evaluating risk from MP/NP exposure is the presence of co-contaminants. For example, plastics are known to contain a number of additives with significant toxic potential and can also sorb or retain contaminants of concern, such as inorganic arsenic, lead, or perfluoroalkyl sulfonate (PFAS). The presence of these co-existing contaminants will alter, perhaps dramatically so, the toxicity and risk profile associate with the “parent” MP/NP. Thus, the mechanisms of toxicity from NP/MP and associated contaminants on microbes can be attributed to the interactions with intracellular receptors such as the aromatic hydrocarbon receptor (AhR) and peroxisome proliferator-activated receptor γ, which in turn activate intracellular and extracellular metabolic signaling and oxidative stress signaling pathways (Rummel et al. 2019). This pathway activation results in metabolic dysregulation, decreases cell viability or even causes death. Given this complexity of exposure, the mechanisms of toxicity, as noted above, are multifaceted and the assessment of risk is intrinsically difficult.

3 Beneficial effects of MP/NP exposure in terrestrial environment

Notably, MPs/NPs are complex carbon-based materials and as such, exposure may actually convey some benefits to select members of the terrestrial microbiome. This is consistent with the co-metabolism process of environmental contaminants in the terrestrial ecosystem, where xenobiotic compounds can be degraded accidentally due to substrate similarity to the conventional analytes; this generates no energy for the organisms though. For example, features such as a relatively rough surface morphology, large specific surface area, and carbon-rich molecular structure provide an amenable substrate and energy source for the growth and reproduction of selected microorganisms as part of the plastisphere. Bacteria, including Pseudomonas, Flavobacteriaceae, Bacillus and, Rhodobacteraceae have been shown to mediate MP/NP biodegradation (Fig. 1) (Seeley et al. 2020). Biodegradation pathways and mechanisms for plastics are equivalent to hydrocarbon degradation, including that: i) microorganisms may adsorb on the plastic surface through hydrophilic or hydrophobic interactions (hydrogen bonds, π-π interactions, and electrostatic interactions) and may result in biofilm formation (Wang et al. 2021); ii) microorganisms then secrete enzymes that facilitate plastic degradation (i.e., hydrolases and oxidases); and iii) plastics-generated degradation products then leach from the surface of MPs/NPs, traverse the cell membrane, and are ultimately converted to CO2 and H2O through the intracellular tricarboxylic acid cycle within the mitochondrial matrix, providing necessary energy and carbon for the growth of microorganisms (Fig. 1) (Li et al. 2023; Peng et al. 2023; Thakur et al. 2023). In addition to plastic direct biodegradation in soil, MPs/NPs as xenobiotic compounds can be degraded accidentally through cometabolism due to substrate similarity to the conventional analytes which generates no energy for the organisms. For instance, a recent study developed that the presence of livestock manure biochar (LMBC) in soil is able to increase the relative abundance of microbes (e.g., Proteobacteria, Deinococcus-Thermus, Firmicutes, Ascomycota Bacteroidetes, and Basidiomycota) close to MPs, increases the abundance of MP-degrading microbes (e.g., Aspergillus, Bacillus, Chryseolinea, Thermobacillus, Luteimonas, and Mycothermus), and thus promotes the degradation of MPs in soil (carbon loss of 50.8% during 60 d mixture of MP to LMBC), highlighting the enhancing microplastics biodegradation during composting using livestock manure biochar (Sun et al. 2022). From source-sink perspective, under suitable temperature and humidity, MPs/NPs (especially MPs) can support a community of microorganisms by providing both physical substrate and carbon-rich molecules for energy (Huang et al. 2021; Ya et al. 2022). This will facilitate for soil to cultivate the microbiome (bacteria, fungi, and Archaea) on terrestrial environment. In addition, higher soil microbial diversity induced by MP/NP presentation is able to occupying some of niches that otherwise are taken by pathogens, resulting in the reduced risk of hospitalization for infectious and parasitic diseases (Banerjee and van der Heijden 2023). Moreover, incredibly diverse microbial community under the presence of MP/NP may also contribute to keep the quality and health of soils, animal, plant, and human health as the largest microbiome reservoir in earth (Banerjee and van der Heijden 2023).

4 Conclusions

In summary, we highlight that more so than other contaminant groups, the presence of plastics, plastics additives, and co-contaminants greatly complicate the risk calculation for MPs/NPs in terrestrial environments. Given the fact that almost every microorganism in the environment is mixed with other kinds of microorganisms in the ecosystem, and there are interactions among them, such as mutualism, parasitism, antagonism, predation and competition. As some populations are inhibited with the presence of MPs/NPs, others will increase simultaneously. For instance, Ya et al. (2022) developed the effects of PE MPs on soil microbial community and discovered that, in comparison with blank controls, 1% (w/w) of PE MPs promoted the abundance of Proteobacteria (35.1% on Day 7 vs. 29.6% on Day 0), while decreased the abundance of Acidobacteriota (5.6% on Day 7 vs. 10.7% on Day 0) and Firmicutes (2.9 on Day 7% vs. 4.8% on Day 0) at the phylum level (Ya et al. 2022). It is not because the plastics are conveying benefit directly but because more sensitive species are decreasing, which frees up resources from less competition, including microbial colonization, enrichment composition, and energy sources (carbon sources and nitrogen sources) and facilitate for the growth and reproduction of soil microorganism species. Those changes then will have additional consequences, including shifts in predator species and nutrient cycling and redox conditions, and ultimately affecting the basic microbial community structure. It is all incredibly fluid and dynamic and dramatically complicates an assessment of risk. Since, more efforts should focus on the dynamics impacts of toxicity and benefit of MP/NPs on the microbiome in terrestrial environment.

Although many efforts have demonstrated that the ubiquitous presence of MPs in soil environments has the capacity to alter soil microbial diversity (Gkoutselis et al. 2021; Zhu et al. 2022), limited efforts has concerned the temporal dynamics of soil microbial community structure in response to microplastics, leading to the long-term temporal impact of MPs on ambient soil microbial communities and related biogeochemical processes is not fully understood (Wang et al. 2020a). Therefore, we appealed more efforts concerning the impact of MPs/NPs on terrestrial microbiome structure and function on a longer-term scale in the future. Considering the critical role of microorganisms in biogeochemical and energy cycling across global terrestrial ecosystems, a more comprehensive assessment of the risk for MPs/NPs on these organisms must be undertaken, accounting for the concepts of dose and co-contaminants, as well as the dynamics of toxicity and benefit. The specific contents for further studies that need to be addressed are as follows: i) short and long-term dose response (prokaryotes and eukaryotes soil microbiome function) of MPs/NPs to soil microbial community structure; ii) combination impact of plastics coupled with plastics additives or co-contaminants (that spans environmentally relevant concentrations) on the MP/NP risk calculation in soil ecosystem; this should include microcosm studies that enable assessment of 'omic' parameters over the long term, as well as detailed assessment of impacts on soil microbiome function. We also need to understand impacts on eukaryotic microbes, and iii) microcosm studies that enable assessment of 'omic' parameters with long-term MP/NP exposure.