Abstract
Microplastics (MPs) have emerged as a widespread environmental contaminant, raising growing concerns about their impact on terrestrial ecosystems. This comprehensive review paper highlights the effects of MPs on soil properties, soil organisms, and plants, shedding light on the complex interactions within these critical components of terrestrial environments. In terms of soil properties, plastics, ranging from macroplastics to mesoplastics, microplastics, and nanoplastics, have been found to exert significant influence. They can alter soil physical attributes, including texture, structure, bulk density, water aggregate stability, water holding capacity, and rainwater infiltration. Microplastics can affect soil chemical properties by influencing pH levels, electrical conductivity, nutrient cycling, and enzyme activity, and even can cause heavy metal accumulation in plants. These alterations in soil properties have far-reaching implications for ecosystem health and agricultural productivity. Furthermore, microplastics have substantial repercussions on soil organisms, particularly earthworms, collembolans, and microbial communities comprising bacteria and fungi. These organisms play pivotal roles in nutrient cycling and soil health. Microplastics can disrupt their habitats, affect their behavior, and potentially lead to changes in soil biota composition, with widespread effects throughout the terrestrial food web. Microplastics influence plant growth and development; even the microplastic can be uptaken and translocated within plant tissues. Food safety and ecosystem dynamics are affected by these effects. This review paper emphasizes the urgency of understanding the complex interactions between microplastics and terrestrial ecosystems. It highlights the need for further research to comprehensively assess the extent and implications of microplastic contamination in various soil types, under different environmental conditions, and concerning diverse plastic characteristics. Standardized methodologies for studying these interactions are essential to facilitate comparisons across studies.
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Introduction
In a world where plastic has become an inseparable part of our lives because of its convenience, low cost, high durability, waterproofing, good elasticity, and hygiene (Kim et al. 2020b; Wang et al. 2022a; Li et al. 2022b; Xiang et al. 2022), its impact stretches far beyond what meets the eye penetrating even the very ground beneath us. Because of the many benefits associated with plastics, they are used in various industries like buildings, packaging, household goods, electronics and electrical appliances, auto parts, and agricultural goods (Kim et al. 2020b; Xiang et al. 2022). Now, a world without plastics is unimaginable. The first synthetic product was Bakelite, introduced in the early twentieth century. Besides the military, plastic use was not widespread until World War II (Geyer et al. 2017).
In the packaging industry, plastic use is increasing day by day as the world shifted from reusable plastics to disposable plastics, which are ultimately ending up in municipal solid waste; as a result, municipal solid waste (by mass) increased from less than 1% in 1960 to 10% in 2005 in the middle & high-income countries (Geyer et al. 2017). In 1950, plastic production was 2 million tonnes (Mt), and in 2018, it was 359 Mt, which showed a growth of 8.4% annually (Kim et al. 2020b). Reportedly, till 2019, there was 368 Mt of plastic and plastic products production globally (Li et al. 2022b), and only China produced 114 Mt and 59 Mt by Europe, that’s going to increase by two folds by 2040 (Sharma et al. 2023).
(Geyer et al. 2017) reported that 8300 Mt had been produced till the time of his report. And 6300 Mt of plastic waste had been made from 1950 till 2015; around 12% has been incinerated, 9% has been recycled, and 79% (4900 Mt) ended up in landfills or the natural environment. If the current rate continues, 12,000 Mt of plastic waste will end up in landfills or the natural environment (Geyer et al. 2017). Many researchers think that soil is a giant sink or dump yard or plastic waste compared to oceans due to the more significant release of plastics into the terrestrial environment (de Souza Machado et al. 2018; Rochman 2018; Helmberger et al. 2020; Kim et al. 2020b). According to an estimate, 4–23 folds of more plastics are added to terrestrial ecosystem compared to aquatic (Li et al. 2022b). Only 1% of global plastic waste is added to the oceans; the rest is deposited in the soils and freshwater (Zhang and Liu 2018). According to (Wang et al. 2022a), 90% of plastic waste enters the soil ecosystem directly and indirectly.
Plastics are further classified based on their size: macroplastics (> 25 mm), mesoplastics (5–25 mm), microplastics (1–5 mm), and nanoplastics (1–100 nm) (Sharma et al. 2023). Some researchers further classify microplastics as large microplastics (1–5 mm) and small microplastics (1 μm—1 mm) (Kim et al. 2020b). Some researchers also classify microplastics as primary microplastics (tiny in size and used in cosmetics, clothing, fish nets, shampoo, and medical purposes) and secondary microplastics (produced by the fragmentation/degradation of microplastics) (Zhang and Liu 2018; Li et al. 2022b; Sharma et al. 2023). Primarily, scientists define microplastics generally as under 5 mm (Ryan et al. 2009; Law and Thompson 2014; Rillig 2018; Rillig et al. 2018; Rochman 2018; Helmberger et al. 2020). In this paper, we will only discuss the microplastics.
In the ocean, microplastics were reported in the early 1970s (Carpenter and Smith Jr. 1972; Colton Jr. et al. 1974; Helmberger et al. 2020). And (Rillig 2012) discussed microplastics in the soil for the first time about a decade ago (Helmberger et al. 2020). Microplastic pollution in soils is increasing day by day; in extensively polluted top soils, reports have indicated microplastic concentrations reaching as much as 7% of the total weight (de Souza Machado et al. 2018). Similarly, Australian industrial soils 300 mg kg−1 to over 67,000 mg kg−1 (around 6.7% microplastic per total soil weight) (Rillig 2018). The abundance of microplastics at different locations in the world can be seen in Table 1. Annually, “63,000–430,000 and 44,000–300,000 tonnes of microplastics could being added in the soils of farmlands of Europe and North America”, respectively (Nizzetto et al. 2016b, a).
Microplastics can disturb soil ecology, be taken up by plants, disturb nutrient cycling, reduce soil quality/health, and enter the food chain. Microplastics can act as persistent pollutants, stay in the soil for long because of their anti-degradation property/behavior, and adversely affect soil properties. Microplastics might also absorb detrimental contaminants from the soil solution and subsequently concentrate them in the soil (Rillig 2012; Zhang and Liu 2018; Iqbal et al. 2020; Qi et al. 2020; Elbasiouny et al. 2022; Zhang et al. 2022a). In this paper, we will study the impact of MPs on soil properties (physical, chemical, and biological/ biota) and the response of plants to them.
Sources and transport of microplastics towards soils
Microplastics can be added to the soil intentionally and unintentionally. While using plastic film mulch and plastic in fertilizers, we are adding microplastics intentionally. The example of unintentional deposition of microplastics can occur in soil when using sewage sludge, compost, fermented organic wastes, and irrigation with the water from the contaminated water bodies (de Souza Machado et al. 2018; Iqbal et al. 2020; Elbasiouny et al. 2022; Joos and De Tender 2022; Zhang et al. 2022a). And atmospheric deposition (like tire abrasion, deposition of industrial and consumer plastic waste, etc.) of microplastics is also reported even in very remote places, even at high mountains (Scheurer and Bigalke 2018; Cao et al. 2021; Yu et al. 2021c; Joos and De Tender 2022; Li et al. 2022b). Flooding can also cause the deposition of MPs in the soil (Scheurer and Bigalke 2018).
Using sewage sludge as an irrigation source adds more microplastics into the soil compared to oceans annually (Scheurer and Bigalke 2018). According to an estimate, 125 to 850 tons of microplastics per million inhabitant are being added to the European agricultural soils (Nizzetto et al. 2016a). Reportedly, up to 4,196 to 15,385 microplastic particles can be in the per kilogram of the sludge (Mahon et al. 2017; Li et al. 2022b). According to an estimate, 50% of the sewage sludge is being used as fertilizers in developed countries in Europe and North America (Nizzetto et al. 2016a; Sharma et al. 2023), and sewage sludge is also being used as a fertilizer and irrigation source in developing countries like Pakistan (Azam et al. 1999; Keskin et al. 2009). In China, 0.156 Mt MPs are transported to the environment by the sludge (Li et al. 2018b).
Untreated wastewater contains microplastics at a very high rate from washing clothes using detergents and effluents from personal care products. Using this type of wastewater for irrigation purposes can add microplastics to the soil (Li et al. 2022b). Over 90% of MPs are captured in sewage sludge during wastewater treatment. The efficiency of capturing these MPs relies on their particle size and density. Both primary and secondary treatment phases of sewage treatment primarily trap microplastics that have a higher density than water.
Further refinement occurs in tertiary filtration, where larger buoyant particles are successfully eliminated. As anticipated, microplastic particles that are smaller and lighter are discharged with the treated wastewater. In other words, sewage sludge treatment plants could be more efficient in eliminating MPs (Nizzetto et al. 2016a; Yu et al. 2021c).
Even compost can contain up to 14–895 microplastic particles kg−1 (Li et al. 2022b). In the U.S., synthetic fibers were found in the soils where organic waste material was applied (Zubris and Richards 2005). Particle counts ranging from 14 to 895 per kilogram of dry weight were observed (using a conservative estimate where 1 kg of compost comprises around 50% dry weight content) for microplastic particles larger than 1 mm (Weithmann et al. 2018).
Plastic film mulch provides many benefits: controlling weed growth, increasing the soil and air temperature, minimizing soil erosion, reducing evaporation and other water losses, preventing soil splashing, and growing produce quality and yield (Sintim and Flury 2017; Qi et al. 2020; Qiang et al. 2023). Plastic film mulch is another way of adding MPs to soil (Wan et al. 2019; Qi et al. 2020; Qiang et al. 2023) because they are not readily biodegradable (Rillig 2012; Sintim and Flury 2017). (Zhou et al. 2020a) reported the abundance of MPs in the mulched soil with the plastic film (over 570 pieces/kg) compared to the non-mulched (260 pieces/kg) soil. At a cotton field that was mulched for a long time, it was observed that the area covered with the mulch for 5 years, 15 years, and 24 years continuously, the mean abundance of MPs was 80.3 pieces/kg soil, 308 pieces/kg soil, and 1075.6 pieces/kg soil, respectively (Huang et al. 2020). As a result of residual polyethylene mulch film degradation, phthalate esters and di-(2-ethylhexyl) phthalates may form, as well as aldehydes and ketones (Liu et al. 2014). (Wang et al. 2013; Serrano-Ruiz et al. 2021) reported that the agricultural plastic films may be a significant source of Phthalic acid esters (PAEs) contamination in soil and bis-(2-ethylhexyl) phthalate (DEHP), di-n-butyl phthalate (DnBP), and di-n-octyl phthalate (DnOP) were the most abundant phthalate esters. Hence, the primary cause of the harmful impact of microplastics on plants is the microplastics themselves, along with additives like PAEs.
Mostly demanded/used plastic products that are being used and ultimately add MPs to the environment are high-density polyethylene (HDPE), low density polyethylene (LDPE), linear Low Density Polyethylene (LLDPE), biodegradable poly (3-hydroxybutyrate-co-3-hydroxyvalerate) (PHBV), polyethylene (PE), acrylic (PP&A) fibers, polyvinyl chloride (PVC), polypropylene (PP), polyurethane (PUR), polystyrene (PS), polytetrafluorethylene (PTFE), polyethersulfone (PES), polyethylene terephthalate (PET), synthetic blend rubber (SBR), polyurethane (PU), acrylonitrile butadiene styrene (ABS), styrene butadiene (SBR), expanded polystyrene (EPS), thermo-plastic elastomers (TPE), styrene-acrylonitrile copolymer (SAN), poly methyl methacrylate (PMMA), polycarbonate (PC), and polyamide (PA) (Geyer et al. 2017; Scheurer and Bigalke 2018; Kim et al. 2020b; Ya et al. 2021; Wang et al. 2022b; Qiang et al. 2023).
Impact of MPs on soil’s physical properties
Microplastics alter the soil microclimate and atmosphere (de Souza Machado et al. 2018). Microplastics affect soil’s physical properties, including texture, structure and aggregate stability, porosity, bulk density, water holding capacity (WHC), saturated hydraulic conductivity, and reduce rainwater infiltration (Liu et al. 2017; Tang 2020; Joos and De Tender 2022; Zhang et al. 2022a; Li et al. 2022b). It was observed that polyester fibers increased the WHC compared to the polyethylene fibers with increasing concentrations (de Souza Machado et al. 2018; Iqbal et al. 2020; Tang 2020; Sharma et al. 2023).
Contradictory results are also observed by (Guo et al. 2022); reduced WHC was observed in clay to a greater extent than in loamy and sandy soils. The decreased WHC indicates that MPs' negative effect exceeded the micropores' positive impact. The decreasing infiltration rate was observed with the increasing MPs, but it still depends on particle size (Guo et al. 2022). In this case, positive effect of soil’s macropores for infiltration increased compared to the negative impact of MPs on filling macropores (Herath et al. 2013). In this case, the positive effect of soil's macropores for infiltration increased compared to the negative impact of MPs on filling macropores (Guo et al. 2022). If small MPs fill the micropores, this will weaken the soil's water retention capacity (Zhang and You 2013; Guo et al. 2022). Despite increasing the soil's surface area, small microplastic particles might also increase its hydrophobic surface area, which induces water repellency, limit capillary flow, and also adsorb hazardous contaminants (Głąb et al. 2016; Xiang et al. 2022; Qiang et al. 2023). In addition, the water repellency of microplastics in soil and delayed wetting caused by "mixed particles" results in more air replacing water molecules in the pores (Głąb et al. 2016). MPs interfere with the accumulation of small soil particles, reducing micropores (Liu et al. 2017).
Reduction in soil bulk density depends on the types of MPs (Li et al. 2022b); polyester fibers show a decrease in the soil bulk density compared to polyacrylic and polyethylene microparticles; incorporation of MPs like PS, PP, PET, PES, or HDPE at the concentration of 2% (w:w) reduce the bulk density (Iqbal et al. 2020; Tang 2020; Joos and De Tender 2022; Sharma et al. 2023). The decline in the bulk density also has benefits like increased or better soil aeration, penetration, and growth of roots (Rillig et al. 2019). These MPs create channels that can facilitate the movement of water. Water will move along the surface of MPs instead of spaces between the pores, and this can lead to increased water evaporation; this evaporation will increase more and more with the increasing concentration of MPs, this can increase dryness and make conditions harsh for the plant growth (Rillig et al. 2018, 2019; Wan et al. 2019; Iqbal et al. 2020). (Zhichao et al. 2015) reported that plastics can restrict the movement of soil water and solutes.
Fine-textured clay soil has good soil structure, is more tightly arranged, and has a large number of micropores (McCauley et al. 2005); as we will add the low concentration of MPs it will increase porosity and it will be beneficial for the crop growth, but it will no longer beneficial if the concentration of MPs will increased (Wan et al. 2019; Cao et al. 2021), increased MPs will surround soil particles this gesture can alter the pore size distribution (Głąb et al. 2016). With a rise in microplastic concentration (> 1%), the cohesion among microplastics, soil particles, and aggregates could progressively result in the encasement of soil particles by microplastics, akin to a "wrapping" effect; this will reduce the interaction between soil particles. In particular, the formation of these "ineffective pores" through the combination of soil and microplastic particles could potentially displace the "effective pores" that naturally occur between soil particles, causing more air to replace the water in pores, further weakening water permeability (Guo et al. 2022).
Desiccation cracking in soil is a complex physical phenomenon affecting strength, stability, and permeability. As water evaporates, the matric suction within the soil rises as its water content decreases, inducing tensile stress within the soil. The formation of shrinkage cracks on the soil surface occurs when tensile stress at the soil surface exceeds the soil's tensile strength. The shrinkage and cracking characteristics of the soil are related to soil liquid limit. For soils with a low liquid limit, the tensile stress in the soil tends to be less than the tensile strength, so desiccation cracks cannot form. Desiccation cracking was observed when 5 and 10 mm plastics were applied, while desiccation shrinkage's increased rate was observed at 2 mm(Wan et al. 2019). It is easier for soil to develop desiccation cracking when large plastics are present. By forming cracks in the soil, soil water evaporates from the deep soil, leading to further shortages of soil water. When water re-saturates the soil after cracking, plastics and other pollutants can migrate into deep soil layers along the crack (Rillig et al. 2017a).
Microplastics can be found in the deep and top soil; top soil provides a favorable environment for their degradation/breakdown (Elbasiouny et al. 2022). Based on the soil structures, MPs can move downward in fine-textured soils. This movement is not significant, but in coarse-textured soils, this movement is possible because of agricultural practices like plowing, desiccation cracking, bioturbation, or preferential flow. Contaminants can also move down through these cracks/desiccation cracking. Generally, these MPs can’t reach the groundwater but may be possible in coarse-textured soils with high water table (Scheurer and Bigalke 2018; Wan et al. 2019; Xiang et al. 2022).
Incorporation of large MPs like microfibers (HDPE, polyester, and polyacrylic fibers) can decline water-stable soil aggregates (de Souza Machado et al. 2018; Boots et al. 2019; Tang 2020; Zhang et al. 2022a; Li et al. 2022b; Qiang et al. 2023). Microplastics like PE can decrease soil sorption capacity, initiate the movement of organic contaminants, and cause soil hardening, which increases input costs (Qiang et al. 2023). If MPs get sorbed to the soil particles or incorporated into soil structure, then these MPs will not be available to plants and soil biota for uptake (Rillig 2012); that’s a plus point.
Impact of MPs on soil’s chemical properties
Microplastics can affect the soil’s pH, EC, and nutrient cycling, ultimately reducing soil fertility (Scheurer and Bigalke 2018; Qi et al. 2020; Tang 2020). MPs can increase soil pH (Qi et al. 2020; Joos and De Tender 2022), but this can vary from soil to soil like PE lower pH in acidic soils and increase pH in alkaline soils (Dissanayake et al. 2022). (Smolders and Degryse 2002) found out that tire debris can raise soil pH. On the other hand, HDPE can decrease soil pH (Boots et al. 2019).
Nutrients in the soil primarily originate from the breakdown of minerals and organic materials. Enzymes are crucial in governing nutrient cycles, serving as vital indicators of soil fertility. Nutrient profiling can be altered by MPs (Tang 2020; Li et al. 2022b; Sharma et al. 2023). As in the nitrogen (N) cycle, there are different processes like mineralization, immobilization, ammonia volatilization, nitrification, and denitrification (Hanif 2023). There are several enzymes like nitrate reductase, nitrite reductase, GOGAT, glutamine synthase, alanine aminotransferase, and glutamate dehydrogenase (Kishorekumar et al. 2020), and MPs target these enzymes, especially urease and acid phosphatase to affect N cycle (Li et al. 2022b). Fei and coworkers found out that PE and PVC stimulated the activities of acid phosphatase and urease, on the other hand, inhibited the fluorescein diacetate hydrolase activity (Fei et al. 2020). Likely, a reduction in the activity of leucine aminopeptidase (involved in the N cycle) and N-acetyl-b-glucosaminidase was observed under the influence of PS and PE (Awet et al. 2018; Bandopadhyay et al. 2019), and plastic film mulch can affect the N cycle and reduce inorganic N contents (Li et al. 2022b). PP presence boosts the urease enzyme's activity, which ultimately can affect N hydrolysis (Huang et al. 2019). Due to the effects of Polylactic acid (PLA), which is a biodegradable plastic, a reduction in Ammonium (NH4) and increased concentration of nitrate (NO3−) and nitrite (NO2−) was observed (Chen et al. 2020a; Iqbal et al. 2020), increased concentration of NO3− and NO2− may lead to the N losses (Hanif 2023).
Microplastics (5% weight/weight) impacted denitrification, increasing N2O released after a 30-day exposure. This could be attributed to the accelerated rate of NO3− reduction facilitated by microorganisms (Ren et al. 2020). On the other hand, MPs didn’t show any effect on nitrification, and corn starch and copolyester plastic didn’t negatively impact nitrification (Bettas Ardisson et al. 2014; Bandopadhyay et al. 2018).
On the other hand, PA, poly-acrylonitrile, and polyamide can increase the availability of N (de Souza Machado et al. 2019). Contradictorily, phthalate esters can contaminate soil (Iqbal et al. 2020). Prolonged use of plastic mulch can reduce organic matter content and inorganic N. Plastic mulch use for ten years downregulated the gene expression of crucial soil enzymes (sDHA, S-UE, S-b-GC, S-Chi, cbbL, chi-A and b-glu), as well as decrease urease activity (Qian et al. 2018). More importantly, gene abundance related to N2O reduction (nosZ), denitrification (nirS), and N2 fixation (nifH) was elevated, while the denitrification gene (nirK) was decreased (Iqbal et al. 2020). Reportedly, in maize (ZTN 182), polymer-coated fertilizer (PCF) and MPs can stimulate the activities of acid phosphatase, urease, phytase, and nitrate reductase activities (Lian et al. 2021). In soil, phytotase catalyzes phytate hydrolysis to release organic phosphorous for plant growth (Lian et al. 2021). Further effect of MPs on enzyme activities can be seen in Table 2.
Microplastics comprise carbon (C), primarily inert C, making them degrade slowly. Several studies are evident that MPs can alter the C cycle and the transport of other nutrients like N and phosphorous (P) with the aid of dissolved organic matter (DOM); reportedly MPs can increase the dissolved organic carbon (DOC), N, and P, PP and PE can increase the DOM by 72–324% (Liu et al. 2017; Qi et al. 2020; Joos and De Tender 2022; Li et al. 2022b). A high concentration of MPs increases the nutrient content of DOM. Polystyrene accumulate the humic substances comprising high molecular weight contents, so the DOM comprises high molecular weight humic substances or humic-like materials (Liu et al. 2017) under the influence of PP MPs higher concentration (7% w:w to 28% w:w; particle size < 180 μm) of dissolved C, N, and P get accumulated in the soil (Liu et al. 2017; Joos and De Tender 2022). Microplastics can harm the enzymes associated with the C, N, and P cycling, like N-acetyl—glucosaminidase, phosphatase, β-D-glucosidase, cellobiosidase, and N- acetyl-β-glucosaminidase (Elbasiouny et al. 2022).
In the presence of MP fibers (0.4% w/w), detrimental effects of MPs were observed on potassium (K), sulfur (S), and magnesium (Mg); on the other hand, increased zinc (Zn) was observed (Lehmann et al. 2019). Microplastics (polyethylene and poly-butylene adipate-co-terephthalate) can increase soil organic carbon (SOC), which works as an energy source for microbes (Iqbal et al. 2020). Inert C in MPs increases their stability, serves as a C pool, and helps microbes cope with pressure (as it can be an energy source for them) (Rillig et al. 2018).
Microplastics can increase the C:N ratio, which increases microbial immobilization (Rillig et al. 2019). It is reported that MPs can absorb chemical substances and transport them (it can also increase the exposure of these substances to soil organisms), like pesticides, heavy metals, antibiotics, and other xenobiotics, although this adsorption depends on the type of MPs, chemical substances, and environmental conditions, furthermore, MPs can act as a carrier for pathogens (Li et al. 2018a; Rillig et al. 2018; Wan et al. 2019; Yang et al. 2019; Yu et al. 2021c; Zhang et al. 2022a). This adsorption can be beneficial, and those pollutants or chemical substances will be less available to plants and soil biota to uptake; this will be a safe play for soil biota and plants (Rillig et al. 2019). (Yang et al. 2019) reported that MPs like LDPE can transport the pesticide residues to the earthworms, and also promote the input of pesticide residues in soil, and also helps in the transport of glyphosate from the upper soil to the deeper soil (Rodríguez-Seijo et al. 2018b; Yang et al. 2019). Tetracycline and ciprofloxacin, which incorporate carbonyl groups, are superiorly adsorbable to polyamides. As a result of the hydrogen bonds formed between the carbonyl group of the microplastics and its amide group, the microplastics serve as proton donors (Li et al. 2018a). A study revealed that MPs could adsorb heavy metals and contaminated MPs like cadmium (Cd), Zn, nickel (Ni), lead (Pb), silver (Ag), mercury (Hg), iron (Fe), antimony (Sb), and manganese (Mn) (Wang et al. 2022a). Microplastics can also extend the retention time of additional stressors introduced to soils. As a result, prolonged exposure and subsequent adaptation can occur (Sun et al. 2018).
Impact of MPs on soil’s biological properties & soil biota
Soil organisms, especially microbial communities, are indispensable for the future of life on Earth. They regulate many ecosystem functions like organic matter decomposition, nutrient recycling, soil-borne disease suppression, toxin removal, and plant growth promotion (Qi et al. 2020; Joos and De Tender 2022). Microplastics can affect the abundance and diversity of soil organisms (earthworms, collembolans, springtails, isopods, nematodes) and also affect the diversity, structure, sustainability of microbial communities, and the activities of microbes (bacteria and fungi) (Rillig 2012; de Souza Machado et al. 2018; Iqbal et al. 2020; Zhang et al. 2020a; Lin et al. 2020; Kim et al. 2020b; Elbasiouny et al. 2022; Joos and De Tender 2022; Li et al. 2022b; Tunali et al. 2023). MPs can affect soil organisms' growth, reproduction, gut microbiota, and mortality because of organ damage, nutritional imbalance, weak immune system, and metabolism (Wan et al. 2019; Zhang et al. 2020a; Kim et al. 2020b).
(Lin et al. 2020) reported that LDPE application in the soil can alter the composition and abundance of microarthropods and nematode communities. Still, the effects of MPs were also observed on the structure and biomass of the microbial community.
Microplastics consumption by earthworms can pass to the food chain, as it plays a vital role in the soil food web (Elbasiouny et al. 2022; Joos and De Tender 2022). Even earthworms can ingest, digest, and transport MPs downward from top soil to deep in the soil profile possibly; they can reach groundwater (Rillig et al. 2017b; Zhang et al. 2020a; Elbasiouny et al. 2022; Joos and De Tender 2022). There are several species of earthworms like Eisenia fetida, Lumbricus terrestris, Eisenia andrei, etc., on which the effect of MPs has been tested (Joos and De Tender 2022).
Due to the MPs in L. terrestris, reduced growth and higher mortality rate were observed, and in E. andrei, no harmful effects were observed on their survival, reproduction, and body weight (Huerta Lwanga et al. 2016; Rodriguez-Seijo et al. 2017). Reportedly, PS MPs at the concentration of 1% inhibited earthworm growth, while at the concentration of 0.25–0.5%, no significant effect was observed (Ya et al. 2021; Yu et al. 2021c). A study by (Rillig et al. 2017b) revealed that in the presence of L. terrestris, four different sizes of MPs were used; in the presence of earthworms, MPs are found deep in the soil, and this distance can increase as the size of MPs decreases. Moreover, microplastics (MPs) can induce skin lesions and diminish the reproductive rates of earthworms.
In a study conducted on L. terrestris, L. terrestris were exposed to 0.1% and 1% polyester-derived MPs for 35 days, and dried plant material was used as a food source. The results show that MP ingestion was not lethal to L. terrestris, but under the influence of 1% MPs, 1.5 fold decrease in the cast production, 23.4 fold increase of metallothionein-2 (mt2), and 9.9 fold decline in heat shock protein (hsp70) was observed (Prendergast-Miller et al. 2019). In a similar study, the effect of PE MPs was observed on L. terrestris, different concentration (0, 7, 28, 45, and 60%) of PE; after 60 days, a higher mortality rate and reduced growth rate was observed in 28, 45, and 60% PE particles (Huerta Lwanga et al. 2016).
Similarly, when Enchytraeus crypticus was exposed to two different size ranges of nylon (3–18 and 90–150 μm) and PVC, the ingestion was, although not leather for E. crypticus. Still, it affected their reproduction; small-sized nylon particles affected most compared to the large-sized nylon particles; on the other hand, no significant effect of PVC was observed (Lahive et al. 2019). In a separate investigation involving E. crypticus subjected to nano-PS plastic exposure, significant alterations were observed in the intestinal microbiota of these soil dwelling organisms. In addition to essential elements cycles, these microbial communities utilize organic substances. Within the intestinal microbiota of E. crypticus, there was a notable reduction in Flavobacteria, Rhizobium, and other fungal species when exposed to a high concentration of nano-polystyrene plastic microspheres (10%). Furthermore, this exposure resulted in a corresponding decrease in the weight of E. crypticus by 10% (Zhu et al. 2018a).
E. fetida was also exposed to PE and PS at different concentrations for 14 days, at 20% of MPs increased activity of peroxidase and catalase CAT), and the level of lipid peroxidation was observed, contradictorily, the activities of glutathione S-transferase and superoxide dismutase (SOD) were inhibited (Wang et al. 2019b). Huerta Lwanga and his colleagues revealed the presence of LDPE MPs within the soil, earthworm casts, and chicken feces, and the concentration of MPs was increased from soil to earthworm casts and chicken feces. This study brings to light the reality that microplastics (MPs) have gained the capacity to infiltrate and disrupt terrestrial food webs(Huerta Lwanga et al. 2017b). (Zhou et al. 2020c) discovered that earthworms and Cd will decrease their growth and mortality rates. (Zhang et al. 2020b) found out ~ 2 particles/individual PE MPs in earthworms.
According to some theories, the latter effect may result from damage to the male reproductive system. Microplastics consumed by earthworms can trigger the production of nanoplastics (NPs) by interacting with their gut microbiome. These NPs are subsequently released into the environment as smaller plastic particles. Upon excretion, these particles become accessible to other soil-dwelling organisms, such as smaller decomposers like microarthropods. Springtails exposed to MPs can suffer severe consequences, including reduced mobility and increased mortality. These springtails can also carry the microplastics to deeper soil layers (Joos and De Tender 2022). (Zhu et al. 2018c) reported that when Folsomia candida (a collembolan, but informally it is also known as springtail) was exposed to 0.1% PVC MPs, retarded growth and reproduction was observed, and MPs also altered the microbial diversity in the gut of F. candida compared to the surrounding soil. Another study on F. candida revealed that the intestinal microbial community gets altered at 0.5% PE MPs, while at 1%, reproduction was reduced by 70.2% (Ju et al. 2019). In isopod Porcellia scaber, exposure to MPs did not affect food intake, body weight, or energy intake, even after 14 days of exposure (Kokalj et al. 2018).
In the case of Caenorhabditis elegans, MPs are not only ingested by them but also affect/disturb their survival, reproduction (fewer offsprings under the influence of PLA, LDPE, and polybutylene adipate-co-terephthalate (PBAT)), behavior (increased speed, frequency of body bending, and head thrashing), and the blockage of the digestive tract or exert oxidative damage to intestinal tissues. As nematodes were highly dependent on the water films or water-filled pores, MPs can change the soil water dynamics, affecting the performance of nematodes. The maximum MP size that can be ingested by them is 4.4 ± 0.5 μm (Lei et al. 2018b; Lin et al. 2020; Mueller et al. 2020; Joos and De Tender 2022).
In some cases, microbes are used to biodegrade MPs like Bacillus sp. Strain 27 and Rhodococcus sp. Strain 36 isolated from the mangroves (Auta et al. 2018). On the other hand, some fungi can reduce the hydrophobicity of MPs because some fungi promote the formation of the chemical bond between functional carbonyl, carboxyl, and ester groups (Yuan et al. 2020). Furthermore, some HDPE- fungi, like Tubegensis VRKPT1 and Aspergillus flavus VRKPT2, like those used for polyethylene degradation (Devi et al. 2015). Effects of MPs on microbial activities or rhizosphere microbiome vary by MPs shape, size, and soil type. Linear plastics affect microbial activities more commonly than non-linear plastics (Iqbal et al. 2020; Qi et al. 2020; Sharma et al. 2023). Microplastics residues affect the wheat's rhizosphere microbiome (Qi et al. 2020). Low density polyethylene (LDPE) can affect microbial communities' structure, cause oxidative stress, and alter energy metabolism; on the other hand, HDPE can affect the activities of microbial communities and reduce the biomass of earthworms (Qiang et al. 2023).
Further effects of MPs on microbial communities (bacteria and fungi, their diversity, and other soil organisms can be observed in Tables 3, 4, and 5. In some cases, microbes and microarthropods degrade MPs and help in the mitigation of soils polluted with plastics (Qiang et al. 2023); the effect of MPs on soil organisms like earthworms, collembolans, isopods, and nematodes can be seen in Tables 6, 7, and 8. In the gut of larvae insect Tenebrio molitor, two strains of bacteria (Acinetobactor sp. NyZ450 and Bacillus sp. NyZ451) are found; they can help to remove LDPE up to 18% (Yin et al. 2020). Similarly, in the gut of Plodia interpunctella, bacteria presence can help to degrade PE films by around 6–10% (Yang et al. 2014). The bacteria genera Enterobacter, Bacillus, and Pseudomonas are frequently encountered in the biodegradation of plastic materials (Zhang et al. 2022a).
Soil organisms can colonize MPs because of their lower density and hardness and seem softer in texture. This colonization can change soil microbial communities’ composition, like the increased population of N fixers (Burkholderiaceae and Betaproteobacteriales) and reduced population of bacteria for xenobiotic biodegradation (Xanthobacteraceae and Sphingomonadaceae) (Zhang et al. 2022a; Qiang et al. 2023). Another study says that the addition of MPs decreased the abundance of nitrate reductase (nirS) and ammonia-oxidizing bacteria, and a little effect of MPs was observed on the functional genes of ammonia-oxidizing archaea, nitrous oxide reductase, and nitrite reductase (nirK) (Gao et al. 2021). MPs can affect the root symbiont relationship, including mycorrhizal fungi and N fixers; these changes can affect the plant's growth and diversity as it is contributed by the soil microbial diversity and root colonizing (Rillig et al. 2019; Tang 2020).
(Gao et al. 2021) conducted a study, and he found that CO2 fluxes increased at 28.67% with the addition of 18% of MPs in soil. These CO2 fluxes and MPs resistant microbial species (Amycolatopsis, Mortierella, Mycobacterium, Nocardioidaceae, and Aeromicrobium) had a strong and positively correlated relationship.
Plastic film mulch such as PE decreases the abundance of Proteobacteria and increases Actinobacteria (Zhang et al. 2022a). Plastic mulches increase or decrease microbial activity in the winter and summer seasons, respectively; mulches increase temperature in the winter season that will touch the optimal temperature for microbes, while in the summer seasons, increasing temperature more than optimal will limit microbial activity. The limited available studies indicated higher microbial abundances, increased respiration rates, and elevated enzyme activities in the presence of biodegradable plastic mulches (BDMs) compared to PE treatments (Bandopadhyay et al. 2018).
Response of plants
Microplastics affect plants in different ways, hindering seed germination and root growth, causing oxidative stress, inhibiting plant height, low seed setting, reducing plant biomass, inhibiting the water and nutrient uptake, accumulation of MPs in plants, by reducing the photosynthesis rate, altering cell membrane, and by affecting plant-symbiont relationship (Gao et al. 2019; Rillig et al. 2019; Iqbal et al. 2020; Elbasiouny et al. 2022; Li et al. 2022b). Various types of microplastics (MPs) exhibit varying effects on the growth of plants, as demonstrated in experiments involving Lactuca sativa, Triticum aestivum, Allium fistulosum, and Phaseolus vulgaris. These effects encompass reduced biomass, altered growth rate/responses, impacts on productivity, and modifications to community structure (Elbasiouny et al. 2022). In addition, microplastics are bound to plant roots by adhesive secretions and accumulate near root-soil interfaces, leading to elevated concentrations of microplastics. Consequently, an increase in the amount of hydrophobic soil particles may negatively impact crop growth by blocking water and nutrient uptake (Lian et al. 2021; Guo et al. 2022).
The mechanism of MPs taken up by the plants is still unclear, but a couple of methods can help with that, like endocytosis, apoplastic transport, and crack-entry mode (Wu et al. 2021). Endocytosis is a broad term that refers to the cellular process by which cells absorb external materials by engulfing or internalizing them with the cell membrane (Flaherty 2012). (Bandmann et al. 2012) reported that nanobeads with the size of 20 nm and 40 nm were engulfed by the BY-2 cells through endocytosis. Only smaller particles can be internalized because of the endocytic vesical’s 70 nm to 180 nm diameter. On the other hand, BY-2 protoplast cells can internalize large-sized beads even of 1000 nm.
Once particulate plastics enter plant roots, some particles become trapped within the mucus layer, primarily composed of highly hydrated polysaccharides. This process concentrates the particles on the surface of the roots before they are transported within plant tissues via apoplastic transport. The primary driving force behind apoplastic transport is the transpirational pull, which significantly facilitates the distribution of particulate plastics throughout the plant's tissues. However, the apoplastic route from the cortex to the vascular bundle encounters an obstacle known as the endodermic Kasparian strip, which hinders the penetration of pollutants. Consequently, contaminants on the apoplastic pathway are compelled to traverse the endodermic plasmalemma (Wu et al. 2021). A study on Arabidopsis thaliana revealed that nanoplastics entered the stele through the apoplastic pathway (Sun et al. 2020).
The mechanisms involved in how plants uptake particulate plastics were studied, revealing a potential pathway for these particles to bypass the apoplastic route and enter wheat (T. aestivum) plants. Plant cell wall pores and intercellular plasmodesmata typically have diameters of 3.5–5.0 nm and 50–60 nm, respectively. This means that plastics larger than 5 nm cannot penetrate the plant cell wall, and those larger than 60 nm cannot diffuse into the intercellular spaces (Wu et al. 2021).
However, it was observed that particulate plastics, such as those with a size of 200 nm, managed to breach the cell wall through the root cap mucilage, which trapped them in the root cell wall. During periods of active cell division, the apical meristem tissues exhibited high porosity, allowing the diffusion of particulate plastics through these tissues. Furthermore, some cracks could form between epidermal cells and at lateral root sites during cell separation, potentially providing a path for microplastics (e.g., 2.0 μm) to penetrate the stele. Once within the stele, particulate plastics could be transported to aboveground parts of the plant through the xylem, driven by the transpiration stream (Wu et al. 2021). Polymethylmethacrylate, PE, and PS microplastics enter the stele of the root of wheat and lettuce at the site of lateral root emergence; under the influence of transpirational pull, they can be transported to shoots. It creates an alarming situation for the upper parts of plants that can reach the food chain (Qiang et al. 2023).
Microplastics size, shape, type, and concentration affect the plants differently (Tang 2020; Wu et al. 2021; Yu et al. 2021c; Elbasiouny et al. 2022), as shown in Tables 9, 10, and 11. (Sun et al. 2020) found out that positively charged PS can be uptaken by the plans more compared to the negatively charged ones. The type of plastic film used had a strong effect on wheat growth; it can be affected more by the BDM than LDPE (Qi et al. 2018). In Vicia faba, MPs with the size of 100 nm can cause more severe oxidative stress and genotoxic compared to the 5 nm sized MPs, which also block the cell wall pores, resulting in disturbance in the nutrient transport (Jiang et al. 2019).
Moreover, MPs can affect plants at community, individual, and cell levels (Wu et al. 2021). At the community level, MPs can alter the plant synergetic interaction; if it becomes out of balance, few species will dominate the ecosystem functions. For example, in Europe, changed bulk density and increased soil macroporosity under the influence of microfibers. The shoot and root mass of grasses and herbs increased, which can increase Calamagrotis invasion, and allelophatic Heieracium became a dominant species (Wu et al. 2021).
On an individual scale, MPs can affect the plant’s physiological and biochemical properties (Wu et al. 2021). Microplastics inhibit seed germination in cress (Lepidium sativum). Microplastics block the seeds' capsules and reduce root growth (Iqbal et al. 2020; Wu et al. 2021; Joos and De Tender 2022). Synthetic fiber and biodegradable PLA also retard seed germination (Tang 2020). Linear Low Density Polyethylene (LLDPE) inhibits seed germination and bud length at low concentrations, but at high concentrations, contradictory behavior was noted; LLDPE increased germination (Qiang et al. 2023). High-density polyethylene (HDPE) suppressed the germination of wheat seeds, but in another study, HDPE didn’t suppress the germination of Mung bean seeds but reduced the bud length, root length, fresh weight, and moisture content of the seedlings (Qiang et al. 2023). Further effects of different MPs on seed germination can be observed in Tables 9, 10, and 11. (de Souza Machado et al. 2019) reported the increased root length, area, and biomass in the onion (Allium fistulosum) under 2% polyethylene high density (PEHD), PS, PET, PA, PP, and PES. Under the influence of 1% LDPE and 1% starch-based BDM root mass decreased in wheat (Triticum aestivum) significantly also affected the above ground and below ground parts of wheat during reproductive and vegetative growth phases. Biodegradable plastic mulches (BDMs) negatively affected wheat growth more than LDPE (Qi et al. 2018).
Microplastics can affect photosynthesis indirectly; MPs can affect the leaves, show sign of inhibited growth, MPs will hinder chlorophyll fluorescence, reduce chlorophyll a and b, imped protein synthesis modulating energy, affect amino acid metabolism, and interferes with the antioxidant defense system of plants. Although, the effect of MPs on leaves remains less significant than on roots (Gao et al. 2019; Wu et al. 2021; Li et al. 2022b).
Microplastics can affect plants on the cell level (Wu et al. 2021). In their 2019 study, Zhang and colleagues showcased a notable reduction in hydroxybenzoic acid levels induced by polystyrene (PS), resulting in changes to cell wall compositions in spinach (Spinacia oleraceae) plants, also inducing metabolic reprogramming in leaves and roots at high doses, and induce stronger metabolic reprogramming in leaves compared to the high amount (Zhang et al. 2019). Reactive oxygen species (ROS) serve as vital indicators in investigating cytotoxic effects, capable of causing harm to cellular structures and functions, as highlighted by (Zhang et al. 2011). Frequently, nanoplastics are implicated in the generation of ROS, leading to oxidative stress (when the ROS level exceeds the antioxidative activities of the organisms) in higher plants and algal cells. When exposed to ROS stress, particulate plastics can lead to a downregulation in ROS-related metabolic processes. Moreover, ROS stress may negatively impact a plant's genetic integrity (Wu et al. 2021). While in lettuce (Lactuca sativa L. var. ramosa Hort), MPs impact the growth and physiology due to an increased ROS content in leaves and roots which will lead to increased antioxidant enzymes like SOD and CAT (Gao et al. 2019).
Studies conducted on wheat revealed that when wheat was exposed to PS microplastics, no significant effects of MPs were observed on wheat seedlings, but MPs decreased the accumulation of cadmium and cuprum because of the sorption of these heavy metals to MPs; in this scenario, MPs prevent plants from the toxic effects of heavy metals, and this will improve photosynthesis, increase chlorophyll content, and reduces the ROS accumulation (Zong et al. 2021). Contradictorily, chlorophyll content and dry biomass were decreased in the case of maize under the influence of biodegradable polylactic acids (PLA) at a high dose. At the same time, PE showed no phytotoxicity (Wang et al. 2020a). In another study, when exposed to PE, MPs declined the transpiration rate, nitrogen content, and maize growth (Urbina et al. 2020). Similarly, when Lolium perenne (perennial ryegrass) was exposed to PLA, this reduced the germination and suppressed the shoot length; alteration in root biomass was also observed (Boots et al. 2019).
Conclusion
Microplastics and nanoplastics are an emerging global concern, resulting from the range of anthropogenic activities, with the limited understanding of their effects on soil and terrestrial plants. Despite the many benefits of plastics, as per the previous studies, plastics (macroplastics, mesoplastics, microplastics, and nano plastics) presence in the soil will have adverse effects on soil physical (texture, structure, bulk density, water aggregates stability, water holding capacity, and rainwater infiltration) and chemical properties (alter pH, EC, affect nutrient cycling, enzymes activity, and cause the accumulation of heavy metals in plants) of soil. MPs also affect the soil biota, like earthworms, collembolans, springtails, isopods, and microbes (bacteria and fungi).
There are several ways by which these substances could influence plant performance. The effects can be positive or negative; they can increase root growth and heavy metal accumulation in soil biota. These consequences vary depending on the specific plant species involved, potentially resulting in shifts in plant community composition. And it's also depending on the size, shape, and type of microplastics because each can affect the terrestrial ecosystem differentially. Determining the size and direction of these effects across different scales, from individual plants to entire ecosystems, will pose a challenge contingent upon factors such as ecosystem type and the extent and nature of contamination. It is crucial to conduct research to test these effects, as plants play a significant role in the climate system. The impact of microplastics on plants, including their uptake and potential translocation within plant tissues, emphasizes the need for a comprehensive understanding of the implications for food safety and ecosystem health. While some studies suggest possible negative consequences, there is still much to uncover regarding the mechanisms and long-term effects on different plant species.
We must also explore/understand the interaction of MPs, soil, soil organisms, and plants. Once MPs are uptaken, they can enter the food chain; who knows what will result from this move. Who knows how plants and microbes will interact with them? We still don’t know much about the impact of MPs on the community structure of microbes and root-colonizing microbes. Very little research is available on it; that’s not enough because many cycles and mechanisms work in the soil, as the soil is a complex entity. Many more questions need to be addressed. Even if we keep the rest of the plastic aside and only talk about the biodegradable plastic mulches, we know the short-term impacts and residues in soil, but the long-term effects are still unknown. The relationship between plastics and microbes needs more exploration because different plastic polymers behave differently, even in the case of biodegradable mulches. The additives used in the production of plastic products and their effects on plants are unknown and need more research to explore their interaction with the world underneath the soil surface.
As we navigate the challenges posed by microplastics in our soils and ecosystems, addressing this issue is vital for preserving the health and integrity of our terrestrial environments, safeguarding agricultural productivity, and ensuring a sustainable future for future generations.
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Muhammad Nauman Hanif: Designed the study, developed the team, and contributed majorly to the original draft's write-up. Nazish Aijaz, Khadija Azam, Waham Ashaier Laftah, and Ian B. Benitez participated in the write-up (according to their expertise) and were assigned authorship positions as per their contribution). Muhammad Akhtar, Muhammad Babur, Waham Ashaier Laftah, and Nabeel Kadhim Abbood supervised the study and helped in proofreading.
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Hanif, M.N., Aijaz, N., Azam, K. et al. Impact of microplastics on soil (physical and chemical) properties, soil biological properties/soil biota, and response of plants to it: a review. Int. J. Environ. Sci. Technol. (2024). https://doi.org/10.1007/s13762-024-05656-y
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DOI: https://doi.org/10.1007/s13762-024-05656-y