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Environmental Pollution 313 (2022) 120167

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Degradation of polylactic acid/polybutylene adipate films in different ratios


and the response of bacterial community in soil environments☆
Yalin Zhang a, Wei Gao a, b, Aoyun Mo a, Jie Jiang a, b, Defu He a, b, c, d, *
a
School of Ecological and Environmental Sciences, East China Normal University, Shanghai, 200241, China
b
Shanghai Engineering Research Center of Biotransformation of Organic Solid Waste, East China Normal University, Shanghai, 200241, China
c
Shanghai Key Laboratory for Urban Ecological Processes and Eco-Restoration, East China Normal University, Shanghai, 200241, China
d
Technology Innovation Center for Land Spatial Eco-restoration in Metropolitan Area, Ministry of Natural Resources, Shanghai, 200062, China

A R T I C L E I N F O A B S T R A C T

Keywords: Biodegradable plastic mulch film (BDM) is an environmentally friendly alternative to conventional polyethylene
Biodegradable plastic film mulch, and has been growingly used in agriculture. However, practical degradation performance of BDM,
Soil especially the widely used type of blended polylactic acid (PLA)/polybutylene adipate (PBAT) in different ratios,
Polylactic acid
and microbial alteration in soil environments, remain largely unrevealed. In this study, four types of BDM
Polybutylene adipate
Bacterial community
blended with 40–80% PLA and 20–60% PBAT were comparatively investigated through microcosm soil incu­
bation experiments for 105 days, and combined with conditions of different soil moisture or pH. Microbiome
within film-surrounding soil were assayed using 16 S rRNA high-throughput sequencing. Results showed a trend
of increasing degradation efficiency with the increase of PLA proportion, and 70% PLA and 30% PBAT group
presented the highest weight loss rate, i.e., 60.16 ± 5.86%. In addition, degradation and aging of PLA/PBAT
varied among different soil moisture and pH values. A moderate moisture, i.e., 60% and a neutral pH7.0 caused
significantly high degradation efficiency compared to other moisture or pH conditions. Moreover, bacterial
abundance and community structure in the surrounding soil were related to soil moisture and pH. PLA/PBAT
incubation treatment induced a remarkable increase in abundance of degradation-related species Pseudomonas
and Sphingomonas. Bacterial richness and diversity in soil correspondingly respond to ratio-different PLA/PBAT’s
degradation under moisture/pH-different conditions through a redundancy analysis. Altogether, these findings
indicate that practical degradation of PLA/PBAT film is closely related to soil environments and bacterial
community. It is significant for the application of biodegradable plastics in agriculture on the perspective of soil
sustainability.

1. Introduction increased nearly 230 times since 1981 (Xue et al., 2021). Biodegradable
plastics have been proposed as one of the dominant strategies to alle­
The application of plastics in agriculture has positive economic ef­ viate plastic pollution (Viera et al., 2021). Biodegradable plastic film can
fects, such as better crop quality and the increase of food production, but be partially or completely degraded by microorganisms, which is
it also leads to irreversible plastic contamination in agricultural eco­ considered as a promising alternative product for PE mulching film
systems (He et al., 2018; Gao et al., 2019). Conventional plastic such as (Filiciotto and Rothenberg, 2021). Biodegradable plastics can be divided
polyethylene (PE) and polypropylene (PP) were largely applied in into biological- and petroleum-based polymers, mainly includes poly­
greenhouses, tunnels, and mulching in agricultural activities (Plastic lactic acid (PLA), polyhydroxyalkanoate (PHA), polybutylene adipate
Europe, 2020). Among them, plastic mulching film had a most heavy (PBAT), polycaprolactone (PCL), and so on (Melchor-Martinez et al.,
application, and was a major source of plastic residues in agricultural 2022). Currently, plastic film has been gradually used in agriculture, and
soil (Li et al., 2022b). In China, the total amount of agricultural global market of mulching film has accounted for about 56.80% of
mulching film per year has reached up to 137.9 million tons, has agricultural plastic film market, it is estimated that the global


This paper has been recommended for acceptance by Xiangzhou Yuan.
* Corresponding author. School of Ecological and Environmental Sciences, East China Normal University, Shanghai, 200241, China.
E-mail address: dfhe@des.ecnu.edu.cn (D. He).

https://doi.org/10.1016/j.envpol.2022.120167
Received 7 July 2022; Received in revised form 21 August 2022; Accepted 9 September 2022
Available online 14 September 2022
0269-7491/© 2022 Elsevier Ltd. All rights reserved.
Y. Zhang et al. Environmental Pollution 313 (2022) 120167

biodegradable films will increase to 2.62 × 106 tons in 2023 (European spectrum and carbonyl index. We further analyzed degradation of PLA/
Bioplastics, 2017; Xie et al., 2022). However, there are still knowledge PBAT film under different soil moisture or pH conditions. Finally,
gaps of BDM, especially about practical degradation performance and microbiome within film-surrounding soil were fully assayed; bacterial
environmental risks (Flury and Narayan, 2021; Griffin-LaHue et al., richness and diversity were emphatically analyzed and compared among
2022; Yang et al., 2022). film-different, soil moisture- or pH-different groups. The objective of this
According to EN17033 standard (EN 17033, 2018), BDM should study is to reveal degradation characteristics of different ratio PLA/
meet the request of a degradation rate of 90% within 2 years. A rela­ PBAT film and microbial community’s response in soil environments.
tively short degradation cycle is advantageous for BDM. However, the
growth cycle of major crops is usually in the range of 3–6 months, which 2. Materials and methods
is obviously shorter than the cycle of commercial BDM’s degradation.
Therefore, it is needed to explore the practical degradation of BDM and 2.1. Plastic films and soil
its influencing factors, and possibly synchronizes with the crop growth
cycle. According to previous studies, the biodegradation of BDM largely Four types of different ratio PLA/PBAT films were selected as BDM
depended on the composition of polymer materials, of various degra­ materials. Conventional PE mulching film was simultaneously used as a
dation performance among different types of BDM (Choe et al., 2021). comparative material. These commercial plastic films were purchased
Currently, PLA and PBAT are mostly-widely used BDM in agriculture. from local companies (the detailed shown in Table S1). PLA/PBAT and
However, the application of PBAT is limited due to poor performance in PE film was identified by the method of the infrared spectrum (Nicolet
toughness and weak photo-aging properties (Kanwal et al., 2022a). iS5, Thermo Fisher Scientific). Ratios of PLA and PBAT composition in
Otherwise, PLA has good mechanical properties, processability and biodegradable plastic film were further assayed using thermal gravi­
biodegradability (Taib et al., 2022) and has widely used as mulch, drip metric analyzer (TGA/DSC3+, Mettler Toledo). According to previous
irrigation pipes, and shielded greenhouse tunnels. PLA and PBAT are thermogravimetric analysis method (Xiang et al., 2020), composition
usually blended to improve material performance for meeting the proportions of PLA and PBAT were determined as 40, 50, 70, 80% and
request of agricultural film (Gigante et al., 2019). Previous studies have 60, 50, 30, 20% in four types of BDM, respectively (Fig. S1). Agricultural
demonstrated that the degradation of single PLA or PBAT was related to soil was collected from farmland in Huai’an, Jiangsu Province in May
their molecular structure, purity, and crystallinity (De Ho et al., 2019; 2021. Physical and chemical properties of soil including electrical con­
Choe et al., 2021). However, practical degradation performance of ductivity, pH value, organic matter content, and bulk density were
blended PLA/PBAT, especially of different ratios as agricultural measured according to previous methods (Nelson and Sommers, 1982;
mulching film, remains largely unrevealed. Klute and Dinauer, 1986; Capka et al., 2009). Three parallel experiments
Currently, blend ratios of PLA/PBAT mulch were mostly based on run for each parameter (Detailed shown in Table S2).
production property, but rarely linkage with practical soil environments
(Izzati et al., 2020; Wu et al., 2021). Physical and chemical properties of 2.2. Plastic film degradation and experimental groups
soil, such as moisture, temperature, and pH varied greatly (Yuan et al.,
2020; Chen et al., 2022). Degradation of PLA/PBAT film would be Soil was naturally dried for 48 h, and then filtered through a 2000
influenced by these soil factors, and mulching treatment would in turn μm-size sieve to remove big debris. The soil was filled in a series of
affect soil properties. For instance, degradation ability of PBAT was glassware (about 90 g soil in each glassware), and used for degradation
largely different in different types of soil (Han et al., 2021). In addition, experiment of plastic film. Ratio-different PLA/PBAT films and PE films
soil moisture and pH varied greatly among different regions. For were cut to small pieces in an uniform size of 4.5 × 4.5 cm, and then
example, soil moisture and pH were respectively reported in the range of respectively buried 2 cm below the surface of soil in glass wares. Each
30–90% and 5.0–9.0 in China (Zhu et al., 2019; Li et al., 2020). glassware only contained a plastic piece, all experimental treatments
Therefore, it is needed to explore practical degradation of PLA/PBAT and controls were set up in triplicate. These containers were sealed with
film under conditions of different soil moisture and pH. tin foil, which were uniformly perforated in order to ensure a dark and
Microbial communities are crucial to stabilize soil ecosystems and aerobic environment. The whole degradation experiment was per­
plant growth (Isobe et al., 2022; Zhang et al., 2022a). However, appli­ formed for 105 days, and residual film were collected per 15–30 days
cation of BDM can influence soil microbiome (Chen et al., 2020; Li et al., after incubation treatment. The soil incubation and plastic degradation
2022a; Wang et al., 2022a; Zhang et al., 2022b). Previous studies have process was carried out within a clean bench and the temperature was
shown the increase of microbial activity in soil after the use of plastic kept at 25 ◦ C. The soil relative moisture was determined by gravimetric
mulching (Fang et al., 2020; Gomez et al., 2020). Microbial community method, and adjusted to 30–90% based on analysis of relative moisture
in the surrounding soil would be influenced by the application of BDM content, and the soil pH was adjusted to 5.5–8.5 with ferrous sulfate
(Zhou et al., 2021). In addition, BDM could indirectly affect soil mi­ solutions and hydrated lime solutions.
crobial communities through changes in soil microclimate, such as A total of 3 experimental groups were performed in this study,
water, temperature, and vapor diffusion. In turn, the change of micro­ including film-different groups, soil moisture-, and pH- different groups;
bial community would affect the degradation rate of BDM. Polymer corresponding controls without plastic film incubation were simulta­
degradation of biodegradable plastics was absolutely dependent on neously carried out (detailed group information shown in Table S3).
related enzymes microorganisms secreted (Polman et al., 2021; Sanchez, Film-different groups included four types of different ratio PLA/PBAT, i.
2021; Wang et al., 2022b). For example, Brevundimonas and Sphingo­ e., L80/B20, L70/B30, L50/B50, L40/B60, and PE. Soil moisture-
bacterium were proved as main bacteria to degrade PLA/PBAT in different groups included H30, H60, and H90, for 30%, 60%, and 90%
anaerobic digestion plants (Peng et al., 2022). Despite of existing studies moisture for PLA/PBAT(L70/B30) degradation experiment. Soil pH-
on microbial degradation of single PLA or PBAT (Delacuvellerie et al., different groups, i.e., pH5.5, pH7.0, and pH8.5 were also experi­
2021), microbial response to PLA/PBAT films of different ratios in soil mented for degradation of PLA/PBAT film.
has never been investigated, especially linkage with different soil
conditions. 2.3. Determination of weight loss rate of mulching film
In this study, the degradation of agricultural film of PLA/PBAT blend
with different ratios were comparatively investigated through micro­ In experiment, plastic film samples were ultrasonically cleaned with
cosm soil incubation experiments. Degradation efficiency was deter­ distilled water for 3 min, and repeated 3 times. Then, these film samples
mined by morphology changes and mass balance. Oxidation and aging were naturally dried, and fully spread and photographed. After that,
characteristics of PLA/PBAT film were evaluated by the infrared each film was weighed using an electronic balance, and as md (after

2
Y. Zhang et al. Environmental Pollution 313 (2022) 120167

degradation). The original mass of film was mo (before degradation). (Axygen Biosciences, USA), and quantified by Quantifluor St (Promega,
The weight loss rate was calculated as according to following formula USA) according to the manufacturer’s instructions. Then, the purified
(1). Three pieces of film were collected and assayed at each sampling amplicons were combined in equimolar (11 ng DNA/sample) and paired
time for each experiment group. ends on the Miseq platform (Illumina, USA) in terms of the standard
protocol of Majorbio biopharm (Shanghai, China) (Li et al., 2018). On
Weight loss rate (%) = (mo − md ) / mo x 100% Formula (1)
Megson cloud platform, OTU clustering, species annotation,
Alfa-diversity including Shannon and Chao1 index, β-diversity, i.e., a
2.4. Infrared spectrometer analysis and carbonyl index determination non-metric multidimensional scale (NMDS), and redundancy analysis
were carried out for all sample sequences.
After residual film samples were cleaned and dried, then infrared
absorption spectrum of each residual film was gained by Fourier trans­ 2.6. Quality assurance and quality control
form infrared spectrometer (Nicolet iS5, Thermo Fisher Scientific). The
wave number range was set in the range of 4000–400 cm− 1, and the All experiments were carried out in a dry and clean environment.
scanning frequency was 16 times. Three sampling points on each plastic Samples are kept in a dark, aerobic, closed environment to avoid
film were randomly tested. After calibration, the infrared absorption interference from atmospheric fallout. The vessels were rinsed three
spectra were used to calculate the carbonyl index of each group. The times with distilled water and dried before use. In the experiment of
carbonyl index was determined as the ratio of the carbonyl peak area to microbial diversity analysis, sample collection, PCR amplification, and
the reference peak area. The actual spectrum 1770-1690 cm− 1 was set as gene sequencing were strictly according to quality assurance and control
the carbonyl peak for PE, and 1790-1600 cm− 1 was set as that for PLA/ of standard molecular biology (Liao and Chen, 2021).
PBAT film. The reference peak was set at 1500-1400 cm− 1 for PE, and at
1560-1330 cm− 1 for PLA/PBAT (Rudnik and Briassoulis, 2011; Palai 2.7. Statistical analyses
et al., 2021).
SPSS 23.0 software was used for data analysis. All data are expressed
2.5. Microbial diversity analysis as mean ± standard error (SEM). Chao1 index and Shannon index were
respectively used to estimate bacterium community richness and di­
2.5.1. Sample collection versity for indicating α-diversity, which were calculated using QIIME 2
After incubation treatment, about 2–3 g soil sample was collected and visualized by R software v3.2.0. Redundancy analysis (RDA) was
nearly treated plastic film (2 mm above and below) in each glassware. conducted to analyze factors influencing bacterial communities in soil.
Control soil samples were collected at the same depth of soil without The significant differences between different groups were analyzed by t-
plastic film. All experimental and control treatments were set up in test, and multiple groups by one-way analysis of variance (ANOVA). The
triplicate. Samples were stored in a refrigerator at − 80 ◦ C for subsequent p value of less than 0.05 was considered statistically significant. All data
analysis. were mapped using GraphPad prism 6.

2.5.2. DNA extraction 3. Results


According to the product instructions of Fast DNA ® Sample, DNA
was extracted using spin kit for soil kits. The product DNA quality was 3.1. Biodegradation of different ratio PLA/PBAT mulching film
evaluated by 1% agarose gel electrophoresis. Fluorescence quantitative
instrument and spectrophotometer were respectively used to determine After soil incubation treatment, the four types of PLA/PBAT film
the concentration and purity of extracted DNA. presented significant breakage and loss in comparison to pre-treatment
(Fig. 1A). But morphological changes were very slight in PE film. Among
2.5.3. PCR amplification and quality inspection four groups of ratio-different PLA/PBAT, L70/B30 presented the highest
The V3–V4 region of bacterial 16 S ribosomal RNA (16 S rRNA) was weight loss rate, i.e., 60.16 ± 5.86%, followed by L80/B20 with 45.68
amplified by PCR amplifier. Fragment of 515 F (5′ - ± 4.35%, then L50/B50 and L40/B60 with 29.40 ± 2.58% and 17.63 ±
GTGCCAGCMGCCGCGGTAA-3′ ) and 806 R (5′ -GGAC­ 1.84%, respectively (Fig. 1B). Weight loss rates of four PLA/PBAT film
TACHVGGGTWTCTAAT-3′ ) were used as primers for PCR amplification. were markedly higher than that of PE film. During incubation treatment,
The length and concentration of PCR products were detected by 1% weight loss rates were relatively low in the first 60 days; then rise
agarose gel electrophoresis. Samples with bright main bands were used gradually in PLA/PBAT film, especially L70/B30 and L80/B20 groups
for further experiments. PCR reaction contained 25 μL 2x Premix Taq, 1 (Fig. S2A). Finally, there were significant differences in weight loss rates
μL Primer-F (10 μM), 1 μL Primer-R (10 μM) and 50 ng DNA. After among L80/B20, L70/B30, and L50/B50 or L40/B60 group (Fig. 1B).
comparing the concentration of PCR products with genetools analysis Infrared spectrums of pre- and post-treatment plastic film were
software (Syngene, version4.03.05.0), the required volume of each compared in each group (Fig. 1C). Carbonyl index was further used to
sample was calculated according to the principle of equal mass, and indicate oxidation degrees of these films. Results showed that the
mixed with the PCR products. Then, mixed PCR products were recov­ carbonyl index of post-treatment was significantly higher than corre­
ered by e. z.n.a ® Gel extraction kit gel Recovery Kit. After eluted by sponding pre-treatment in all five groups (p < 0.05). After incubation
buffers, target DNA fragments were finally recovered. treatment, the carbonyl index of L70/B30 increased by 1.96 times.
Among four BDM groups, change trend in means of carbonyl index
2.5.4. Library construction and sequencing remained consistent with weight loss rates (Fig. 1B–D). Otherwise, the
Subsequent high-throughput sequencing steps such as library con­ carbonyl index of PE film increased by 7.67 times in comparison to the
struction, quality inspection and on-line sequencing were performed in pre-treatment (p < 0.05).
MEG gene sequencing company (Magigene, Shanghai) on the Illumina
hiseq2500 platform. The V3V4-1 segment (front-end primer sequence 3.2. Effect of soil moisture and pH value on degradation of PLA/PBAT
“actcctacggaggcagca” and back-end primer sequence “ggac­ film
tachvggtwtctaat”) of bacteria in collected samples were sequenced.
We further investigated the impact of soil moisture and pH on
2.5.5. Amplicon analysis degradation efficiency of PLA/PBAT film. Results showed that residual
The AxyPrep DNA gel was used to extract and purify the amplicon Kit BDM varied largely among different moisture or pH conditions (Fig. 2A).

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Y. Zhang et al. Environmental Pollution 313 (2022) 120167

Fig. 1. Degradation characteristics of different-ratio


PLA/PBAT film in soil. (A–B) Morphological
changes (A) and weight loss rate (B) of different types
of films; (C–D) Changes of infrared spectra (C) and
corresponding carbonyl index (D) before and after
soil degradation treatment of PLA/PBAT and PE films;
Data are expressed as standard error of the mean
(±SEM). The letter a, b, c, or d indicates significant
difference compared with the 1st, 2nd, 3rd, and 4th
group. *p < 0.05, **p < 0.01, ***p < 0.001, t-test,
compared to corresponding pre-treatment.

Fig. 2. Effects of soil moisture and pH values on


degradation and aging of PLA/PBAT films in soil.
(A–B) Morphological changes (A) and weight loss
rates (B) of PLA/PBAT films under different soil
moisture and pH values; (C–D) Infrared spectrum (C)
and Carbonyl index (D) changes of PLA/PBAT films.
PLA/PBAT film was mixture of 70% PLA and 30%
PBAT, and was treated of soil incubation for 105 day.
Data are expressed as standard error of the mean
(±SEM). The letter a, b, or c indicates significant
difference compared with the 1st, 2nd, 3rd group. *p
< 0.05, **p < 0.01, ***p < 0.001, t-test, compared to
corresponding pre-treatment.

Obviously, neutral soil environmental conditions caused relatively Oxidation degree of these films was further characterized by their
serious damages or loss of PLA/PBAT film. Statical results showed H60 carbonyl index. Results showed that the carbonyl index of BDM in three
group presented a biggest weight loss, i.e., 60.16 ± 5.86%, followed by moisture-different groups was significantly elevated after incubation
H90 (15.84 ± 0.35%) and H30 group (10.37 ± 0.92%), with significant treatment (p < 0.05), and especially increased 1.96 times in H60 group
differences among the three groups (Fig. 2B). Similarly, pH7.0 group (Fig. 2D). In pH-different groups, significant elevation of the carbonyl
showed the biggest weight loss rate, and then pH5.5 and pH8.5 group of index only occurred in pH7.0 group. In both moisture- and pH- different
13.24 ± 0.68% and 1.98 ± 0.30% loss. In the process of incubation groups, the carbonyl index change was consistent with the trend of
treatment, weight loss rates mainly appeared in the last 45 days weight loss.
(Figs. S2B–C). Then, infrared spectrum of pre- and post-treated PLA/
PBAT film were simultaneously presented and compared (Fig. 2C).

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Y. Zhang et al. Environmental Pollution 313 (2022) 120167

3.3. Bacterial flora in soil after degradation treatment of PLA/PBAT film Results showed that the rda1 and rda2 axis covered 21.69% and 10.30%
of the total variation of bacterial community structure, respectively.
After high-throughput sequencing of microbiome from film- Three groups of variables including PLA proportion, soil moisture, and
incubation soil samples, a total of 2,094,710 valid splice fragments pH were emphatically analyzed correspond to three groups of different
were obtained. The number of valid splice fragments varied in the range experiments. Results showed that the contribution rate of PLA propor­
of 103,897–119,111 among samples. With the increase of dilution per­ tion of BDM was the highest, reaching 57.5% (p < 0.01), followed by soil
centage, richness of bacterial species gradually flattened to a saturation moisture with 26.9% of a significant impact (p < 0.05), and then pH
stage (Fig. S3). The characteristics of dilution curves demonstrated that with 15.7% but of no significance (Fig. 5).
sequencing analysis was relatively accurate, and covered all bacterial
compartments in the samples. Results showed that a total of 325 bac­ 4. Discussion
terial OTUs appeared in all soil samples of different groups. However,
the minimum 672, 2210, and 1079 to the maximum 2974 of unique 4.1. Degradation characteristics of different ratio PLA/PBAT film
OTUs occurred in film-, soil humility-, and pH- different groups
(Fig. 3A). Bacteria were subsequently identified at phyla level. Results The present study revealed different degradation efficiency and mi­
showed that a total of 31 bacterium phyla were contained within these crobial response among different ratio PLA-PBAT mulch films in soil.
samples. Top 20 bacterial phyla in relative abundance were detailly Our results demonstrated a relatively high degradation rate in mulching
shown in Fig. 4B. The bacteria mainly consisted of Proteobacteria films with high-proportion PLA such as 70% and 80%. It indicates PLA
(25.2–77.1%), Bacteroidetes (8.5–16.7%), Actinomyces (2.9–14.3%), and PBAT have various degradation efficiency in the same soil condi­
Chlorotrophomonas (0.3–17.1%), and Acidobacter (0.2–12.9%). Phylum- tion, which would be closely related to their molecule structures and
level analyses showed that microbial community structure varied among special degradation-related microbiome. This is supported by several
film- and soil moisture-different groups. Among them, Proteobacteria previous studies. For example, biodegradation rates of PBAT and PLA in
presented a high abundance in pH-different groups. In addition, Chlor­ the PLA/PBAT blend were lower than those for the respective single
oflex in pH5.5 and pH8.5 group was of a relatively low abundance polymers in freshwater with sediment (Fu et al., 2020). Other studies
proportion, but Firmicutes showed a relatively high proportion in com­ also showed various degradation rates among single and blend PBAT/­
parison to pH7.0 group (Fig. 3B). PLA films (Fu et al., 2020; Xie et al., 2022), which are consistent with the
The bacterial community structure was further analyzed at the genus present study. In view of polymer structures, PLA contains a large
level. A total of 212 genera were identified in all experimental and number of ester groups. The main degradation of PLA occurred mainly
control groups. Major species included Pseudomonas (0.2–15.2%), through the random breaking of the main chain ester groups, and the
Sphingomonas (0.3–10.1%), Citrobacter (0.01–29.1%) and Devosia degradation trend varied among functional groups. In PBAT, soft
(0.02–17.9%) (Fig. 3C). The proportion of dominant bacteria varied aliphatic domain was easier to hydrolyze than rigid aromatic domain
among film-, soil humility-, and pH- different groups. In film-different (Kanwal et al., 2021). The difference of polymer structure would largely
groups, Pseudomonas and Sphingomonas showed high abundance, but decide practical efficiency by the action of soil microbiome. Our results
with slight variance among ratio-different PLA/PBAT groups, despite of first provided degradation data of ratio-different PLA/PBAT film in soil.
obvious difference from the control group. In the moisture- and pH- It is significant to producer or user for environmentally friendly appli­
different groups, we also found relatively high abundance of Pseudo­ cation of PLA/PBAT film.
monas and Sphingomonas in experimental groups, when compared with Moreover, our results disclosed special soil bacteria promoted
corresponding control groups. However, abundance of other microbial degradation of PLA/PBAT film. At the level of genus, Pseudomonas and
species varied among experimental or control groups, without obvious Sphingomonas were found to positively related to the degradation of
characteristics. PLA/PBAT film. Moreover, the abundance of Pseudomonas and Sphin­
gomonas presented an increasing trend with the increase of PLA pro­
3.4. Alpha and beta diversity of soil microbiota respond to PLA/PBAT portion in PLA/PBAT film. It indicates that Pseudomonas and
film Sphingomonas are the key species for the degradation of BDM. It is
supported by several studies about the degradation of BDM. For
According to NMDS ordination analysis, species and related evolu­ example, in BDM field experiment in a Mediterranean apricot orchard,
tionary information of bacterial communities of soil samples in all Pseudomonas putida was isolated from the soil attached to the polymer
groups were rearranged as points on a two-dimensional spatial axis surface (Fontanazza et al., 2021). Bandopadhyay et al. (2020) also
(Fig. 4A). NMDS was well fitted to the relationships between microbial showed that the richness of Methylobacter, Arthrobacter and Sphingomo­
community structures based on Bray-Curtis similarity coefficients. The nas in the soil after use of biodegradable plastic film. In another study,
distance between sample points indicated relationship of microbial Pseudomonas, Flavorbacterium and Rhizobacterium were also considered
community between the samples. Results showed that pH5.5, pH7.0, as potential degradation bacteria for biodegradable plastic films (Liang
and pH8.5 groups’ coverage areas did not overlap, and had relatively et al., 2022). Other studies indicated that PLA-degraded bacteria
large distances. Under the same treatment condition, pH7.0, H30, H60, included Bacillus, Sphingomonas, Pseudomonas, Alcanivorax and Amyco­
and H90 groups’ coverage areas intersected, but did not completely latopsis (Satti et al., 2017; Butbunchu and Pathom-Aree, 2019; Zhang
overlap, with relatively small distances. It demonstrated that structural et al., 2019). These results were consistent with the present study, which
variances of bacterial communities were related to both soil pH and suggest that Pseudomonas and Sphingomonas were major types of
moisture. Furthermore, results showed that both Shannon and Chao1 BDP-degradation bacteria in soil.
index of bacterial communities varied in film-different groups. Among
four types of PLA/PBAT groups, L80/B20 and L70/B30 presented rela­ 4.2. Influencing factors of degradation of BDM
tively high Shannon and Chao1 index in comparison to other BDM or
control groups (Fig. 4B and C). In moisture-different groups, Chao1 The present study disclosed degradation efficiency of PLA/PBAT
index and Shannon index presented an increasing trend with the in­ mulch varied under different soil moisture and pH conditions. Moderate
crease of soil moisture (Fig. 4D and E). Otherwise, Shannon and Chao1 moisture of 60% and a neutral pH were optimal conditions for the
index in pH7.0 group was significantly higher than that in pH5.5 or degradation of BDM. According to a previous study, the degradation rate
pH8.5 group (Fig. 4D and E). of PLA/PBAT blends was relatively slow in natural soil environments
The relationship of bacterial community structure and PLA/PBAT possible due to inappropriate degradation conditions (Agarwal, 2020).
film, soil moisture or pH was further evaluated by redundancy analysis. Soil moisture was considered as a major driver of organismal activity,

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Y. Zhang et al. Environmental Pollution 313 (2022) 120167

Fig. 3. Bacterial flora in soil after degradation treatment of different-ratio PLA/PBAT film under conditions of different soil moisture and pH value. (A) Veen diagram
of bacterial species among soil sample groups (OTU level); (B–C) Bacterial community structure of different-treated soil samples at the phylum (B) and genetic (C)
level. Data are expressed as standard error of the mean (±SEM).

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Y. Zhang et al. Environmental Pollution 313 (2022) 120167

Fig. 4. Inter-group bacterium diversity analysis of soil samples after incubation treatment of PLA/PBAT films. (A) Nonmetric dimensional scaling (NMDS) plots for
microbiome community among soil moisture- and pH-different groups; (B–C) Comparison of bacterial α-diversity by Chao1 index (B) and Shannon index (C) among
film-different groups; (D–E) Chao1 index (D) and Shannon index (E) indicate bacterial α-diversity between moisture- or pH-different groups.

the surface of PLA/PBAT could be inhomogeneously hydrolyzed during


mineralization (Krueger et al., 2015; Kliem et al., 2020). Another study
showed that an appropriate moisture was conducive for the hydrolysis of
polymers. In this process, the ester bond or hydrophilic groups would be
gradually cut and decomposed polymers into small fragments, which
might be used as an additional carbon source for soi microbiome. A
previous study demonstrated that excessive soil water content could
influence the activity of microorganisms, then affect the degradation of
biodegradable plastic film (Rosli et al., 2021). It is consistent with the
present study, together indicating appropriate soil moisture beneficial to
soil microbiome and subsequent degradation of BDM. In another study,
the richness of bacterial community was promoted after the increase of
soil moisture (Liu et al., 2020). Similarly, Pseudomonas had relatively
low the survival rate in low soil moisture (Yasmin et al., 2022). These
supported our results that degradation bacteria Pseudomonas and
Sphingomonas had relatively high abundance under condition of mod­
erate soil moisture.
In addition, the present study demonstrated that pH7.0 condition
induced relatively high degradation efficiency of PLA/PBAT film, as well
as high abundance of related bacterium. It was speculated that the pH
values of 5.5 and 8.5 might exceed the most appropriate pH range of
degradation bacteria for BDM. During hydrolysis, the cleavage of PLA
chain would release H+ and acid monomers. Similarly, PBAT can be
depolymerized to produce water-soluble products such as terephthalic
acid (Zumstein et al., 2018; Fu et al., 2020; Jia et al., 2021; Soulenthone
et al., 2021). Therefore, degradation of PLA or PBAT might change soil
Fig. 5. Redundancy analysis of soil bacterial community (phylum level) and
pH value to a certain degree (Goto et al., 2020; Kanwal et al., 2022b). In
PLA proportion of blended films, soil moisture, or pH value after incubation
turn, pH values would affect bacterial community and degradation ef­
treatment of PLA/PBAT films.
ficiency of BDM. This study provides crucial evidence in detail. Another

7
Y. Zhang et al. Environmental Pollution 313 (2022) 120167

study also proved that potential degradation bacteria Pseudomonas and Wei Gao: Methodology, Investigation. Aoyun Mo: Investigation. Jie
Sphingomonas were significantly enriched in slightly acidic soil (Ma Jiang: Investigation. Defu He: Conceptualization, Methodology, Inves­
et al., 2021), which is in line with our results. Therefore, this study tigation, Validation, Funding acquisition, Project administration,
provides an important reference about influencing factors of BDM′ Writing -review & editing.
degradation, which is helpful for guiding large-scale application of BDM.
Declaration of competing interest
4.3. Environmental implication
The authors declare that they have no known competing financial
The present study has revealed practical degradation characteristics interests or personal relationships that could have appeared to influence
of ratio-different PLA/PBAT film and the response of microbial com­ the work reported in this paper.
munity. These results are significant for producers and users for selec­
tion of PLA/PBAT mulch film in an appropriate blend ratio. This study Data availability
provides crucial evidence of practical degradation efficiency of ratio-
different PLA/PBAT mulch, which would be helpful to guide their pro­ Data will be made available on request.
duction in terms of soil sustainability. In addition, BDM would degrade
too fast or too slow under suboptimal conditions including soil moisture Acknowledgements
and pH, and could not meet the application performance as agricultural
film. In fact, soil property varies globally. For example, in China, This work was supported by the National Natural Science Foundation
moisture of agricultural soil varied in the range of 30–90%, and the pH of China (No. 42277273) and the National Key Research and Develop­
mostly in the range of 5.0–9.0 (Zhu et al., 2019; Li et al., 2020). From the ment Program of China (No. 2018YFC1901004). All authors would
perspective of geographical distribution, soil presented characteristics of appreciate the comments by Dr. W-M Wu, Stanford University.
“wet in the East, dry in the West, acid in the South and alkali in the
north” in China (Han et al., 2020; Zhao et al., 2021). According to our Appendix B. Supplementary data
results, PLA/PBAT mulching film would have various degradation effi­
ciency among these regions. Therefore, use and management policy Supplementary data to this article can be found online at https://doi.
would be correspondingly modulated in terms of local soil conditions. org/10.1016/j.envpol.2022.120167.
We further found remarkable changes of soil microbiome after
application of PLA/PBAT mulch. For example, degradation-related References
Pseudomonas and Sphingomonas obviously increased. Changes of soil
microbiome would alter soil function and fertility, which might have a Agarwal, S., 2020. Biodegradable polymers: present opportunities and challenges in
providing a microplastic-free environment. Macromol. Chem. Phys. 221 (6),
long-term impact on soil sustainability. A previous study showed the use 2000017.
of BDM increased dissolved organic carbon and nitrogen, but decreased Bandopadhyay, S., Gonzalez, J.E.L.Y., Henderson, K.B., Anunciado, M.B., Hayes, D.G.,
active nitrogen in soil (Meng et al., 2021). Mazzon et al. (2022) DeBruyn, J.M., 2020. Soil Microbial communities associated with biodegradable
plastic mulch films. Front. Microbiol. 11, 587074.
demonstrated that BMP increased carbon mineralization and immobi­ Butbunchu, N., Pathom-Aree, W., 2019. Actinobacteria as promising candidate for
lization of available nitrogen after their application. As a carbon source, polylactic acid type bioplastic degradation. Front. Microbiol. 10, 2834.
BDM may have a positive effect on functional microorganisms and soil Capka, D., Kisic, I., Zgorelec, Z., Mesic, M., Jurisic, A., 2009. Determination of soil pH in
dominant soil types in the republic of Croatia. Agric. Conspec. Sci. 74, 13–19.
fertility. Previous studies showed that the application of BDP caused Chen, H.P., Wang, Y.H., Sun, X., Peng, Y.K., Xiao, L., 2020. Mixing effect of polylactic
obvious increase of related bacteria (Chen et al., 2020; Qi et al., 2020), acid microplastic and straw residue on soil property and ecological function.
and even significantly improved soil enzyme activity (Gao et al., 2021). Chemosphere 243, 125271.
Chen, Q.L., Hu, H.W., Sun, A.Q., Zhu, Y.G., He, J.Z., 2022. Aridity decreases soil
Combined with these results, the present study provides an in-depth protistan network complexity and stability. Soil Biol. Biochem. 166, 108575.
observation of interaction of BDM and soil microbiome. With the Choe, S., Kim, Y., Won, Y., Myung, J., 2021. Bridging three gaps in biodegradable
popularization of commercial PLA/PBAT film, the potential impacts on plastics: misconceptions and truths about biodegradation. Front. Chem. 9, 671750.
De Ho, G.X., Zumstein, M.T., Getzinger, G.J., Ruegsegger, I., Kohler, H.P.E., Maurer-
soil properties and microorganisms should be more considered and
Jones, M.A., Sander, M., Hillmyer, M.A., McNeill, K., 2019. Photochemical
researched. transformation of Poly(butylene adipate-co-terephthalate) and its effects on
enzymatic hydrolyzability. Environ. Sci. Technol. 53 (5), 2472–2481.
5. Conclusion Delacuvellerie, A., Benali, S., Cyriaque, V., Moins, S., Raquez, J.M., Gobert, S.,
Wattiez, R., 2021. Microbial biofilm composition and polymer degradation of
compostable and non-compostable plastics immersed in the marine environment.
This study revealed a trend of increasing degradation efficiency with J. Hazard Mater. 419, 126526.
the increase of PLA proportion in PLA/PBAT plastic mulch. Moreover, EN 17033, 2018. Plastics - Biodegradable Mulch Films for Use in Agriculture and
Horticulture - Requirements and Test Methods. European Standard, European
degradation and aging of mulch varied among different soil moisture Committee for Standardization, Brussels, Belgium.
and pH values. A moderate moisture, i.e., 60% and a neutral pH 7.0 were Europe, Plastic, 2020. Plastics – the Facts 2020. https://www.plasticseurope.org/appl
relatively optimal conditions for degradation of PLA/PBAT. Soil bacte­ icat ion/files/5716/0752/4286/AF_Plastics_the_facts-WEB-2020-ING_FINAL.pdf.
Available online European Bioplastics, 2017, June 2017. http://www.european-biop
rial community structure was related to soil moisture and pH. After in­ lastics.org/market/.
cubation treatment of PLA/PBAT film, abundance of degradation- Fang, C., Ke, W.B., Campioli, M., Pei, J.Y., Yuan, Z.Q., Song, X., Ye, J.S., Li, F.M.,
related species, such as Pseudomonas and Sphingomonas, were obvi­ Janssens, I.A., 2020. Unaltered soil microbial community composition, but
decreased metabolic activity in a semiarid grassland after two years of passive
ously elevated. Bacterial richness and diversity were correspondingly experimental warming. Ecol. Evol. 10 (21), 12327–12340.
changed in response to PLA/PBAT′ s degradation under conditions of Filiciotto, L., Rothenberg, G., 2021. Biodegradable plastics: standards, policies, and
different soil moisture and pH values. Collectively, the present study impacts. ChemSusChem 14 (1), 56–72.
Flury, M., Narayan, R., 2021. Biodegradable plastic as an integral part of the solution to
suggests that practical degradation of PLA/PBAT plastic mulch is closely
plastic waste pollution of the environment. Curr. Opin. Green. Sust. 30, 100490.
related to soil environments and bacterial community. It provides a Fontanazza, S., Restuccia, A., Mauromicale, G., Scavo, A., Abbate, C., 2021. Pseudomonas
significant insight on the application of biodegradable plastics on the putida isolation and quantification by Real-Time PCR in agricultural soil
perspective of soil sustainability. biodegradable mulching. Agriculture-Basel. 11 (8), 782.
Fu, Y., Wu, G., Bian, X.C., Zeng, J.B., Weng, Y.X., 2020. Biodegradation behavior of poly
(butylene adipate-Co-terephthalate) (PBAT), poly(lactic acid) (PLA), and their blend
Author contribution in ffreshwater with sediment. Molecules 25 (17), 3946.

Yalin Zhang: Investigation, Formal analysis, Writing – original draft.

8
Y. Zhang et al. Environmental Pollution 313 (2022) 120167

Gao, H., Yan, C., Liu, Q., Ding, W., Chen, B., Li, Z., 2019. Effects of plastic mulching and the systematic transition to a new generation of bioplastics. Polym. Bull. (Berlin) 14
plastic residue on agricultural production: a meta-analysis. Sci. Total Environ. 651, (6), 1203.
484–492. Meng, F.R., Yang, X.M., Riksen, M., Xu, M.G., Geissen, V., 2021. Response of common
Gao, L., Fu, D.D., Zhao, J.J., Wu, W.S., Wang, Z.Z., Su, Y.Y., Peng, L.C., 2021. bean (Phaseolus vulgaris L.) growth to soil contaminated with microplastics. Sci.
Microplastics aged in various environmental media exhibited strong sorption to Total Environ. 755, 142516.
heavy metals in seawater. Mar. Pollut. Bull. 169, 112480. Nelson, D.W., Sommers, L.E., 1982. Total carbon, organic carbon and organic matter. In:
Gigante, V., Canesi, I., Cinelli, P., Coltelli, M.B., Lazzeri, A., 2019. Rubber toughening of Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis, second ed.
Polylactic Acid (PLA) with Poly(butylene adipate-co-terephthalate) (PBAT): Am. Soc. of Agron. Inc. Soil Sci. Soc. Am. Inc., pp. 535–579
mechanical properties, fracture mechanics and analysis of ductile-to-brittle behavior Palai, B., Mohanty, S., Nayak, S.K., 2021. A comparison on biodegradation behaviour of
while varying temperature and test speed. Eur. Polym. J. 115, 125–137. polylactic acid (pla) based blown films by incorporating thermoplasticized starch
Gomez, E.J., Delgado, J.A., Gonzalez, J.M., 2020. Persistence of microbial extracellular (tps) and poly (butylene succinate-co-adipate) (pbsa) biopolymer in soil. J. Polym.
enzymes in soils under different temperatures and water availabilities. Ecol. Evol. 10 Environ. 29 (9), 2772–2788.
(18), 10167–10176. Peng, W., Wang, Z.J., Shu, Y.H., Lu, F., Zhang, H., Shao, L.M., He, P.J., 2022. Fate of a
Goto, T., Kishita, M., Sun, Y., Sako, T., Okajima, I., 2020. Degradation of Polylactic Acid biobased polymer via high-solid anaerobic co-digestion with food waste and
using sub-critical water for compost. Polym. Bull. (Berlin) 12 (11), 2434. following aerobic treatment: insights on changes of polymer physicochemical
Griffin-LaHue, D., Ghimire, S., Yu, Y.X., Scheenstra, E.J., Miles, C.A., Flury, M., 2022. In- properties and the role of microbial and fungal communities. Bioresour. Technol.
field degradation of soil-biodegradable plastic mulch films in a mediterranean 343, 126079.
climate. Sci. Total Environ. 806, 150238. Polman, E.M.N., Gruter, G.J.M., Parsons, J.R., Tietema, A., 2021. Comparison of the
Han, T.F., Liu, K.L., Huang, J., Ma, C.B., Zheng, L., Wang, H.Y., Qu, X.L., Ren, Y., Yu, Z. aerobic biodegradation of biopolymers and the corresponding bioplastics: a review.
K., Zhang, H.M., 2020. Spatio-temporal evolution of soil pH and its driving factors in Sci. Total Environ. 753, 141953.
the main Chinese farmland during past 30 years. J. Plant Nutr. 26 (12), 2137–2149. Qi, Y.L., Ossowicki, A., Yang, X.M., Lwanga, E.H., Dini-Andreote, F., Geissen, V.,
Han, Y.J., Teng, Y., Wang, X., Ren, W.J., Wang, X.M., Luo, Y.M., Zhang, H.M., Garbeva, P., 2020. Effects of plastic mulch film residues on wheat rhizosphere and
Christie, P., 2021. Soil type driven change in microbial community affects Poly soil properties. J. Hazard Mater. 387, 121711.
(butylene adipate-co-terephthalate) degradation potential. Environ. Sci. Technol. 55 Rosli, N.A., Karamanlioglu, M., Kargarzadeh, H., Ahmad, I., 2021. Comprehensive
(8), 4648–4657. exploration of natural degradation of poly(lactic acid) blends in various degradation
He, D., Luo, Y., Lu, S., Liu, M., Song, Y., Lei, L., 2018. Microplastics in soils: analytical media: a review. Int. J. Biol. Macromol. 187, 732–741.
methods, pollution characteristics and ecological risks. Trac. Trends Anal. Chem. Rudnik, E., Briassoulis, D., 2011. Degradation behaviour of poly(lactic acid) films and
109, 163–172. fibres in soil under Mediterranean field conditions and laboratory simulations
Isobe, K., Oka, H., Watanabe, T., Tateno, R., Senoo, K., Shibata, H., 2022. Soil microbial testing. Ind. Crop. Prod. 33 (3), 648–658.
community response to winter climate change is phylogenetically conserved and Sanchez, C., 2021. Microbial capability for the degradation of chemical additives present
highly resilient in a cool-temperate forest. Soil Biol. Biochem. 165, 108499. in petroleum-based plastic products: a review on current status and perspectives.
Izzati, A.N.A., John, W.C., Fazita, M.R.N., Najieha, N., Azniwati, A.A., Khalil, H.P.S.A., J. Hazard Mater. 402, 123534.
2020. Effect of empty fruit bunches microcrystalline cellulose (MCC) on the thermal, Satti, S.M., Shah, A.A., Auras, R., Marsh, T.L., 2017. Isolation and characterization of
mechanical and morphological properties of biodegradable poly (lactic acid) (PLA) bacteria capable of degrading poly(lactic acid) at ambient temperature. Polym.
and polybutylene adipate terephthalate (PBAT) composites. Mater. Res. Express 7 Degrad. Stabil. 144, 392–400.
(1), 015336. Soulenthone, P., Tachibana, Y., Suzuki, M., Mizuno, T., Ohta, Y., Kasuya, K., 2021.
Jia, H., Zhang, M., Weng, Y.X., Zhao, Y., Li, C.T., Kanwal, A., 2021. Degradation of poly Characterization of a poly(butylene adipate-co-terephthalate) hydrolase from the
(butylene adipate-co-terephthalate) by Stenotrophomonas sp. YCJ1 isolated from mesophilic actinobacteria Rhodococcus fascians. Polym. Degrad. Stabil. 184, 109481.
farmland soil. J. Environ. Sci. 103, 50–58. Taib, N.A.A.B., Rahman, M.R., Huda, D., Kuok, K.K., Hamdan, S., Bin Bakri, M.K., Bin
Kanwal, A., Zhang, M., Sharaf, F., Li, C.T., 2021. Enzymatic degradation of poly Julaihi, M.R.M., Khan, A., 2022. A review on poly lactic acid (PLA) as a
(butylene adipate co-terephthalate) (PBAT) copolymer using lipase B from Candida biodegradable polymer. Polym. Bull. 1–35.
Antarctica (CALB) and effect of PBAT on plant growth. Polym. Bull. 1–15. Viera, J.S.C., Marques, M.R.C., Nazareth, M.C., Jimenez, P.C., Sanz-Lazaro, C., Castro, I.I.
Kanwal, A., Zhang, M., Sharaf, F., Li, C.T., 2022a. Polymer pollution and its solutions B., 2021. Are biodegradable plastics an environmental rip off. J. Hazard Mater. 416,
with special emphasis on Poly (butylene adipate terephthalate (PBAT)). Polym. Bull. 125957.
1–28. Wang, Q.L., Feng, X.Y., Liu, Y.Y., Cui, W.Z., Sun, Y.H., Zhang, S.W., Wang, F.Y., 2022a.
Kanwal, A., Zhang, M., Sharaf, F., Li, C.T., 2022b. Screening and characterization of Effects of microplastics and carbon nanotubes on soil geochemical properties and
novel lipase producing Bacillus species from agricultural soil with high hydrolytic bacterial communities. J. Hazard Mater. 433, 128826.
activity against PBAT poly (butylene adipate co terephthalate) co-polyesters. Polym. Wang, Y., Davey, C.J.E., Van der Maas, K., Van Putten, R.J., Tietema, A., Parsons, J.R.,
Bull. 1–24. Gruter, G.J.M., 2022b. Biodegradability of novel high T-g poly(isosorbide-co-1,6-
Kliem, S., Kreutzbruck, M., Bonten, C., 2020. Review on the biological degradation of hexanediol) oxalate polyester in soil and marine environments. Sci. Total Environ.
polymers in various environments. Materials 13 (20), 4586. 815, 152781.
Klute, A., Dinauer, R.C., 1986. Physical and mineralogical methods. Planning 8 (79). Wu, D.D., Huang, A.P., Fan, J., Xu, R.W., Liu, P., Li, G.Q., Yang, S.Y., 2021. Effect of
Krueger, M.C., Harms, H., Schlosser, D., 2015. Prospects for microbiological solutions to blending procedures and reactive compatibilizers on the properties of biodegradable
environmental pollution with plastics. Appl. Microbiol. Biotechnol. 99 (21), poly(butylene adipate co-terephthalate)/poly(lactic acid) blends. J. Polym. Eng. 41
8857–8874. (2), 95–108.
Li, X.X., Shi, S., Rong, L., Feng, M.Q., Zhong, L., 2018. The impact of liposomal linolenic Xiang, S., Feng, L.D., Bian, X.C., Li, G., Chen, X.S., 2020. Evaluation of PLA content in
acid on gastrointestinal microbiota in mice. Int. J. Nanomed. 13, 1399–1409. PLA/PBAT blends using TGA. Polym. Test. 81, 106211.
Li, D.C., Huang, J., Ma, C.B., Xue, Y.D., Gao, J.S., Wang, B.R., Zhang, Y.Z., Liu, K.L., Xie, J.Z., Yan, Y., Fan, S.H., Min, X.Y., Wang, L., You, X.Q., Jia, X.F., Waterhouse, G.I.N.,
Han, T.F., Zhang, H.M., 2020. Soil organic matter content and its relationship with Wang, J., Xu, J., 2022. Prediction model of photodegradation for PBAT/PLA mulch
pH and bulk density in agricultural areas of China. J. Soil Water Conserv. 36 (4), films: strategy to fast evaluate service life. Environ. Sci. Technol. 56 (12),
252–258. 9041–9051.
Li, C.T., Cui, Q., Li, Y., Zhang, K., Lu, X.Q., Zhang, Y., 2022a. Effect of LDPE and Xue, Y.H., Guo, J.B., Li, C., Xu, X.B., Sun, Z.X., Xu, Z.Y., Feng, L.S., Zhang, L.X., 2021.
biodegradable PBAT primary microplastics on bacterial community after four Influencing factors of farmers’ cognition on agricultural mulch film pollution in rural
months of soil incubation. J. Hazard Mater. 429, 128353. China. Sci. Total Environ. 787, 147702.
Li, S.T., Ding, F., Flury, M., Wang, Z., Xu, L., Li, S.Y., Jones, D.L., Wang, J.K., 2022b. Yang, Y., Li, Z., Yan, C.R., Chadwick, D., Jones, D.L., Liu, E.K., Liu, Q., Bai, R.H., He, W.
Macro- and microplastic accumulation in soil after 32 years of plastic film mulching. Q., 2022. Kinetics of microplastic generation from different types of mulch films in
Environ. Pollut. 300, 118945. agricultural soil. Sci. Total Environ. 814, 152572.
Liang, J., Zhang, J.F., Yao, Z.M., Luo, S.Y., Tian, L., Tian, C.J., Sun, Y., 2022. Preliminary Yasmin, H., Bano, A., Wilson, N.L., Nosheen, A., Naz, R., Hassan, M.N., Ilyas, N.,
findings of Polypropylene Carbonate (PPC) plastic film mulching effects on the soil Saleem, M.H., Noureldeen, A., Ahmad, P., Kennedy, I., 2022. Drought-tolerant
microbial community. Agriculture-Basel. 12 (3), 406. Pseudomonas sp. showed differential expression of stress-responsive genes and
Liao, J., Chen, Q.Q., 2021. Biodegradable plastics in the air and soil environment: low induced drought tolerance in Arabidopsis thaliana. Physiol. Plantarum 174 (1),
degradation rate and high microplastics formation. J. Hazard Mater. 418, 126329. e13497.
Liu, H., Gao, H., Wu, M.L., Ma, C., Wu, J.L., Ye, X.Q., 2020. Distribution characteristics of Yuan, X., Qin, W.K., Xu, H., Zhang, Z.H., Zhou, H.K., Zhu, B., 2020. Sensitivity of soil
bacterial communities and hydrocarbon degradation dynamics during the carbon dynamics to nitrogen and phosphorus enrichment in an alpine meadow. Soil
remediation of petroleum-contaminated soil by enhancing moisture content. Microb. Biol. Biochem. 150, 107984.
Ecol. 80 (1), 202–211. Zhang, M., Jia, H., Weng, Y.X., Li, C.T., 2019. Biodegradable PLA/PBAT mulch on
Ma, D., Wang, J., Xue, J., Yue, Z.B., Xia, S.F., Song, L., Gao, H.W., 2021. Effects of soil pH microbial community structure in different soils. Int. Biodeterior. Biodegrad. 145,
on gaseous nitrogen loss pathway via feammox process. Sustainability-Basel. 13 104817.
(18), 10393. Zhang, H.Q., Wu, C.F., Wang, F.Y., Wang, H.T., Chen, G.X., Cheng, Y., Chen, J.P.,
Mazzon, M., Gioacchini, P., Montecchio, D., Rapisarda, S., Ciavatta, C., Marzadori, C., Yang, J., Ge, T.D., 2022a. Wheat yellow mosaic enhances bacterial deterministic
2022. Biodegradable plastics: effects on functionality and fertility of two different processes in a plant-soil system. Sci. Total Environ. 812, 151430.
soils. Appl. Soil Ecol. 169, 104216. Zhang, Y., Ma, J., O’Connor, P., Zhu, Y.G., 2022b. Microbial communities on
Melchor-Martinez, E.M., Macias-Garbett, R., Alvarado-Ramirez, L., Araujo, R.G., Sosa- biodegradable plastics under different fertilization practices in farmland soil
Hernandez, J.E., Ramirez-Gamboa, D., Parra-Arroyo, L., Alvarez, A.G., microcosms. Sci. Total Environ. 809, 152184.
Monteverde, R.P.B., Cazares, K.A.S., Reyes-Mayer, A., Lino, M.Y., Iqbal, H.M.N., Zhao, J.Z., Wang, A.H., Wang, H.J., 2021. Soil moisture memory and its relationship with
Parra-Saldivar, R., 2022. Towards a circular economy of plastics: an evaluation of precipitation characteristics in China region. Chin. J. Atmos. Sci. 45 (4), 799–818.

9
Y. Zhang et al. Environmental Pollution 313 (2022) 120167

Zhou, J., Gui, H., Banfield, C.C., Wen, Y., Zang, H.D., Dippold, M.A., Charlton, A., Zumstein, M.T., Schintlmeister, A., Nelson, T.F., Baumgartner, R., Woebken, D.,
Jones, D.L., 2021. The microplastisphere: biodegradable microplastics addition Wagner, M., Kohler, H.P.E., McNeill, K., Sander, M., 2018. Biodegradation of
alters soil microbial community structure and function. Soil Biol. Biochem. 156, synthetic polymers in soils: tracking carbon into CO2 and microbial biomass. Sci.
108211. Adv. 4 (7), eaas9024.
Zhu, G.F., Pan, H.X., Zhang, Y., Guo, H.W., Yong, L.L., Wan, Q.Z., Ma, H.Y., Li, S., 2019.
Relative soil moisture in China’s farmland. J. Geogr. Sci. 29 (3), 334–350.

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