Biodegradable microplastic increases CO2 emission and alters microbial biomass and bacterial community composition in different soil types
Introduction
Today's world is hard to imagine without plastic. The global production of resins and fibers, from which the known plastic is produced with the addition of additives, increased from 2 Mt. in 1950 to 380 Mt. in 2015 (Geyer et al., 2017). Forecasts show a further increase in production, so that 34,000 Mt. of primary plastic could be produced by 2050 (Geyer et al., 2017). If plastic enters the soil, larger particles often break to smaller ones forming microplastics (MPs), typically defined in a size range < 5 mm (De Souza Machado et al., 2018b). Studies have shown that soil MPs can have impacts on various soil physical and chemical properties as well as on organisms such as earthworms and microbes (De Souza Machado et al., 2018, De Souza MacHado et al., 2018; Huerta Lwanga et al., 2016; Lozano and Rillig, 2020; Wang et al., 2022a; Wang et al., 2022b). Although the fate of MPs in soil receives increasing attention, many questions remain unanswered. In particular, its influence on microbial biomass and soil CO2 emissions is not well understood (Rillig et al., 2021), despite the great importance of soil for the global carbon budget and thus also climate change (Raich and Tufekcioglu, 2000).
After plastic is released into the environment, many of the commonly used types of plastic cannot be degraded in a short time but accumulate in ecosystems. Resistance to hydrolytic and enzymatic degradation is provided by the polymers' carbon skeletons (Ng et al., 2018). Widely used plastic types with high stability are, for example, polyethylene (PE) and polypropylene (PP), for which a very long lifetime is predicted (Kyrikou and Briassoulis, 2007; Ng et al., 2018). In contrast to conventional polymer types, which are produced due to their high resistance to degradation, there are also so-called biodegradable polymers. These have heteroatoms (O, N, S) along their carbon structure, at which hydrolytic or enzymatic reactions can take place, which leads to a significant reduction in the persistence of plastics (Ng et al., 2018). This, in turn, allows microorganisms to absorb the plastic particles, mineralize it to CO2, CH4 and H2O, and to incorporate degradation products into their biomass (Ng et al., 2018). Examples of biodegradable plastics are polylactides (PLA), polycaprolactone (PCL), and polybutylenadipat-co-terephthalate (PBAT) (Ng et al., 2018; Jian et al., 2020). Indeed, for PBAT, Kijchavengkul and Auras (2008) could demonstrate biodegradation caused by microbial degradation and hydrolysis.
Several studies showed that both conventional and biodegradable MPs have an effect on physical and chemical soil properties (De Souza Machado et al., 2018, De Souza MacHado et al., 2018; Wang et al., 2022a; Wang et al., 2022c). For instance, Rillig et al. (2021) reported a significant increase in the number of water-stable soil aggregates and in their mean weight diameter (MWD). As a result, air permeability and oxygen supply increased slightly. De Souza Machado et al., 2018, De Souza MacHado et al., 2018, however, reported contrasting results and found a significant decrease in water-stable aggregates by MPs. Besides physical effects, also changes in soil pH and nutrient concentrations were reported (reviewed by Wang et al., 2022a), though results varied with plastic type, concentration, and size. As microorganisms are strongly influenced by chemical and physical soil properties, MPs have also been reported to alter microbial activity (De Souza Machado et al., 2018, De Souza MacHado et al., 2018) and community composition (Yu et al., 2021; Wang et al., 2022c). As microorganisms are driving the degradation of plastic and the decomposition of soil organic matter, a changed microbial community, biomass, and activity may ultimately also affect CO2 emissions from soil. Indeed, Rillig et al. (2021) reported a significant increase in CO2 emissions by 5 to 26 % caused by MP addition. Also, Zhang et al. (2022) observed that LDPE at a concentration of 1 % increased CO2 emissions significantly by 15–17 %. Yet, lower concentrations showed no significant effect.
Assuming that MPs affect soil CO2 emissions especially through their impact on soil physical properties (cf. Rillig et al., 2021), such as aggregate stability and porosity, soil specific effects may be expected. For instance, the ability of soils to form aggregates considerably depends on their texture: the higher the sand content, the less aggregation (Totsche et al., 2018; Simon et al., 2020). Also, sandy soils are usually already well aerated, leading to the assumption that improved porosity caused by MP addition will not alter soil CO2 emissions as much as in poorly aerated soils. Yet, the soil specific effect of MPs has rarely been considered so far.
Previous studies showed that the effect of MP on soil microorganisms depends on plastic type (Feng et al., 2022; Wang et al., 2022c). Especially biodegradable plastics may result in increasing soil CO2 emissions. This can be explained by its impact on physical and chemical soil properties but also by its degradation, which leads to additional CO2 emissions. For instance, the application of 10 % poly(3-hydroxybutyrate co-3-hydroxyvalerate) (PHBV), which is considered biodegradable, showed an increased CO2 emission from soil, which could mainly be attributed to its degradation (Zhou et al., 2021).
The aim of this study was to investigate the effect of conventional and biodegradable microplastics on soil microbial biomass, bacterial community composition and CO2 emissions. We added two different types of microplastic (LDPE and PBAT) to two soils (sandy loam and loam), in two quantities (0.1 % and 1 % of the dry soil weight), and three size ranges (50–200 μm, 200–500 μm, and 0.63–1.2 mm). We measured soil CO2 emissions, substrate-induced respiration as an indicator of microbial biomass and growth (MBC; Anderson and Domsch, 1978), as well as prokaryotic community composition. We hypothesized that biodegradable PBAT, which is more susceptible to degradation, will increase soil CO2 emissions and biomass and cause more pronounced shifts in microbiome composition in comparison with LDPE. Further, due to their larger specific surface, smaller PBAT particles are more easily accessible to microorganisms and may be more rapidly degraded than coarse PBAT particles. We further hypothesized that MP addition will cause more CO2 release from loamy soil compared to sandy loam soil due to physical impact on soil structure.
Section snippets
Sampling and preparation of soil
The soil used for the study was taken from the premises of the Agricultural Training Institute of the District of Upper Franconia in Bayreuth. From a grassland site (49.9267°N, 11.5476°E) a loam was sampled and from a cropland site (fallow at the time of sampling; 49.9295°N, 11.5545°E) a sandy loam (Table 1). Soil was taken at one location per field side from the top 30 cm with a spade after removal of vegetation. The soil was sieved to 2 mm (smaller soil aggregates stayed intact) and stored at
Soil CO2 emissions
Soil CO2 emissions differed significantly between the two soil types and were on average higher in loamy soil than in sandy loam soil (significant soil type effect; Table 2). Plastic addition had a significant effect on soil CO2 emissions but this effect was dependent on soil type, plastic type, plastic size, and plastic content (significant interaction; Table 2). Treatments with PBAT had on average higher soil CO2 emissions compared with the control when added at high concentration of 1 % (
Does biodegradable PBAT alter soil CO2 emissions, biomass, and microbiome composition more than LDPE?
LDPE amendment did not show any effect on CO2 emissions, suggesting that plastic amendment alone did not affect microbial activity. This is surprising as MPs have been reported to alter porosity, bulk density, and aggregation (De Souza Machado et al., 2018, De Souza MacHado et al., 2018; Rillig et al., 2021), known to affect microbial activity. Yet, both previous studies applied plastic fibers, which may well differ in effect on physical soil properties from the irregular fragmented particles
Conclusion
Plastic is continuously accumulating in soils, including agricultural systems. Therefore, it is relevant to understand and predict how long MPs will remain in the soil and how it affects soil microbial properties. We were able to show that LDPE, classified as a conventional plastic type, does not affect CO2 emissions from two different soils, and that a degradation of LDPE during a time course of four weeks was unlikely. In contrast, PBAT, a biodegradable plastic, was shown to stimulate soil
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was funded as part of the Collaborative Research Center 1357 “Microplastics - Understanding the mechanisms and processes of biological effects, transport and formation: From model to complex systems as a basis for new solutions” by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – SFB 1357 – Grant no. 391977956 – Subproject A06 to E.L. and T.L. We thank Seema Agarwal for providing PBAT (subproject C02 of the CRC1375) and we thank the KeyLab Genomics &
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