Journal of Hazardous Materials 418 (2021) 126329

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Journal of Hazardous Materials

journal homepage: www.elsevier.com/locate/jhazmat

Research Paper

Biodegradable plastics in the air and soil environment: Low degradation

rate and high microplastics formation
Jin Liao a, b, Qiqing Chen a, *
a
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 500 Dongchuan Road, Minhang District, Shanghai 200241, China
b
Shanghai Polar Moment Science and Technology Education Company, Shanghai 200433, China

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

Editor: Dr. R Teresa In recent years, the promotion and use of biodegradable plastics (BPs) are growing into a general trend. Here the
degradation performance of different types of BPs was investigated in the natural environment. Their degra­
Keywords: dation levels followed the order of pure BPs> BP blends> claimed “BP”≈ non-biodegradable plastic after 6-
Biodegradable plastic month incubation. Photo- and biodegradation were the main degradation mechanisms of these plastics in the
Natural environment
air and soil, respectively. Poly(p-dioxanone) (PPDO) exhibited the highest weight loss potentials in both air (54.7
Microplastics
± 9.1%) and soil (56.8 ± 4.8%), due to its special ether bond and the rich and diverse microorganisms on its
Biodegradation
biofilms. The microbiota on PPDO was distinct and enriched with Chloroflexi and Firmicutes that responsible for
carbon cycle and organic degradation. The weight loss was only 1.1–8.0% for poly(lactic acid), and 0.8–6.8% for
poly(butylene adipate-co-terephthalate), and other plastics are basically non-degradable. Of note, numerous
microplastics were formed after PPDO degradation, with 441 ± 326 and 2103 ± 131 item/g plastic in the air and
soil, respectively. Taken together, the monitoring of BP biodegradation in the natural environment is of vital
importance, and it is risky to promote large-scale application of BPs if the knowledge gap of their environmental
behavior has not been well addressed.

1. Introduction
The polymer material industry is developing rapidly at present as it
plays a vital role in human life (Napper and Thompson, 2019; Namazi,
2017), but it also brings some confusion to society. Compared with the
rapid production of plastics, the recycling of plastics is not optimistic
and the accumulation of plastic has brought unprecedented pressure to
the natural environment (Deng et al., 2020; Thompson, 2017; Rochman,
2018). To address these issues, the public is advocating the use of
degradable alternative products for disposable plastics in addition to
developing effective recycling technology (Ghosh and Jones, 2021; Fil­
iciotto and Rothenberg, 2021). Among the degradable plastics, biode­
gradable plastics (BPs) are especially interesting for nondurable
applications and widely used, as they can be biodegraded by microbes
existing in nature to biomass, H2O, and CO2 or CH4 and may effectively
solving the plastic accumulation problem (Haider et al., 2019; Shen
et al., 2020). The mechanisms for biodegradation are mainly driven by
microorganisms, which can first adhere to BPs, utilize the BPs for
assimilation; then the polymer will be degraded through plastic frag­
mentation after hydrolysis; and finally, the BP metabolites and gas
molecules will be released into the environment (Shabina et al., 2015;
Bano et al., 2017).
However, the biodegradation of BPs usually requires relatively high
moisture and temperature conditions, such as the compost degradation
needs 70% humidity moisture and 55 ◦ C (Tabasi and Ajji, 2015), which
are not always reliable in the natural environment. Besides, the abun­
dance of microorganisms also has a significant impact on the degrada­
tion level. For instance, the degradation rate of poly(lactic acid) (PLA) in
the open environment is still debated (Haider et al., 2019; Bagheri et al.,
2017) and polyhydroxyalkanoate (PHA) pellets and films were slowly
degraded with 13–58% degradation after 160 d incubation in the
seawater (Volova et al., 2010). Moreover, the chemical structure and
crystallinity of BPs can strongly affect their biodegradation (Emadian
et al., 2017; Shruti and Kutralam-Muniasamy, 2019). For example, the
BPs with less complexity of structure or lower molecular weight are
more susceptible to microbiota, and enzymatic hydrolysis degradation
accelerates with the decreasing of BP’s crystallinity (Tabasi and Ajji,
2015; Adhikari et al., 2016). Thus, it is difficult to assess the degradation
performance of BPs in the natural environment, only with the degra­
dation data of BPs under standard conditions set by ASTM and ISO

* Corresponding author.
E-mail address: chenqiqing@sklec.ecnu.edu.cn (Q. Chen).

https://doi.org/10.1016/j.jhazmat.2021.126329
Received 16 March 2021; Received in revised form 1 June 2021; Accepted 2 June 2021
Available online 5 June 2021
0304-3894/© 2021 Elsevier B.V. All rights reserved.
J. Liao and Q. Chen
(Kjeldsen et al., 2018), which were not designed to characterize
biodegradation in the open environment but rather to establish the
suitability for organic recycling (e.g., composting). Hence, it is still a
question of whether BPs can be a promising approach to solve the plastic
accumulation problem in a long run, and the investigation and assess­
ment of the degradation processes of BPs and potential formation of
secondary pollutants are largely needed under natural environmental
conditions.
Up to now, the research on ecotoxicological effects of non-
biodegradable microplastics pollution has been widely discussed, and
their potential risks to the environment and human health have been
explored (Besseling et al., 2019; Zhang et al., 2020; Liu et al., 2019).
However, the research on the biological effects of BPs is still in the cradle
stage (Muroi et al., 2016; Yamamoto-Tamura et al., 2015). There is an
absence of standards and test methods for evaluating the biodegrad­
ability of plastic materials within unmanaged freshwater ecosystems
(including lakes, streams, and rivers), and most marine environments
(Harrison et al., 2018). Moreover, secondary plastic particles may
release during BP degradation, and consequently pose potential
ecological risks (González-Pleiter et al., 2019). However, limited studies
have been mainly carried out in the aquatic environment, while re­
searches about BP microplastics formation in other environmental
media (such as the air and soil environment) is relatively scarce. Further,
there is a lack of data on particle concentration of microplastics formed
during BP degradation, which is more valuable for microplastic toxicity
studies.
Moreover, there are various kinds of blends of BPs that are mixed by
two or more BPs to achieve commercially functional properties (Nar­
ancic et al., 2018), which will also affect their degradation performance.
For instance, when PLA is blended with poly (butylene adipate-co-ter­
ephthalate) (PBAT) or cellulose acetate butyrate, the biodegradation
level became lower than that of pure PLA, which was probably due to
the BPs became more hydrophobic (Tabasi and Ajji, 2015; Jain and
Tiwari, 2015). Besides, some types of claimed BPs by merchants, which
are not actually made of biodegradable polymers, are intermingled in
the market and lack sufficient monitoring and regulation. Thus, it re­
mains unclear what are the impacts of BP when discarded (or left as
allowed) in natural environments.
We here, therefore, investigated the degradation processes of four
popular types of BPs and two typical BP blends together with a non-
biodegradable control plastic in the natural air (lack of microorgan­
isms) and soil (rich with microorganisms) conditions, to gain a better
understanding of their potential environmental fate. The weight loss
kinetics of plastics along the 6-month degradation was monitored,
microplastics formation was investigated after degradation, and the
microbial community diversity and degradation mechanisms of
different plastics were discussed in depth.
2. Materials and methods
2.1. Experimental setup
Packaging accounts for the biggest segment of global bioplastics
production with 47.3% in 2020 (European Bioplastics, 2021). In this
study, we selected six kinds of BP or claimed “BP” packaging films to
carry out degradation experiments, including poly(p-dioxanone)
(PPDO), poly(lactic acid) (PLA), poly(butylene adipate-co-tereph­
thalate) (PBAT), 40% mineral doped polyethylene (MD40), PLA_blend
(50% of PLA+50% polyethylene), and PBAT_blend (90% PBAT+10%
PLA). Finally, the polyethylene (PE) packaging film was selected as a
non-biodegradable plastic control, which has the highest demand by
resin type among all the non-biodegradable plastics (PlasticsEurope,
2020). PLA and PBAT are chosen because these two kinds of synthetic
biodegradable aliphatic polyesters have the largest output at present,
which have been widely used in packaging materials (European Bio­
plastics, 2021). But the degradation performance of PLA and PBAT in the
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Journal of Hazardous Materials 418 (2021) 126329
water is poor that their mass loss does not exceed 2% after one year
(Bagheri et al., 2017). Hence, a newly developed BP PPDO is chosen in
this study, which has been proven to have excellent degradation per­
formance even in the water (Yuan et al., 2014). Moreover, BPs are also
commonly blended to offer better functionality, but their environmental
fate has not been fully investigated (Narancic et al., 2018). Besides, as
there is no strict management for the BPs currently, some “claimed” BPs
(whose actual composition does not contain BP) have entered the mar­
ket. Thus, two common blends (PLA_blend and PBAT_blend) and a
typical “claimed” BP (MD40) are also chosen here to investigate their
fate in natural air and soil environments. Information about their
composition, degradation test standards, and environments for them to
disintegrate were listed in Tables S1–S2.
The experiments were carried out in the environment where was
easy to accumulate plastic debris, as we assume that BPs after disposal
are also easy to accumulate there, both in the air (lack of microorgan­
isms) and soil (rich with microorganisms). Our experiments were con­
ducted from May 2nd to November 1st, 2020, at 31◦ 1′ N, 121◦ 27′ E,
Shanghai, China. The temperature, humidity, and rainfall content were
recorded during the whole degradation period (Fig. 1a–c). To avoid
contact with plastic containers and to collect BPs after degradation, we
cut the plastics into 5 cm × 5 cm thin-film slices and placed them into
tailor-made aluminum foil chambers with three replicates for each
sampling point (Fig. 1d).
In the air environment, we put the plastics under a windowsill of our
laboratory, which can not only ensure efficient sunlight irradiation but
also avoid the immersion of rainfalls (Fig. S1). In the soil experiment,
agriculture paddy soil (5–15 cm depth) was used to incubate plastics.
Microbial species in the soil were abundant and distributed in 15 phyla,
among which the abundances of Actinobacteriota, Proteobacteria, Acid­
obacteriota, and Chloroflexi dominated the bacterial community
(Fig. S2). The bottom of the trays has been covered with soil before the
addition of plastic and a 5-cm thickness of soil was covered on the top of
the tray, to ensure full contact between plastic and soil as much as
possible (Fig. S3). The degradation experiments lasted for 6 months, and
we collected samples at 0.5,1, 2, 3, 4.5, and 6 mon, respectively.
2.2. Biodegradable plastic identification
All original BP materials were first observed under a Zeiss micro­
scope (Discovery V8 Stereo, MicroImaging, Germany), and then iden­
tified with a micro-Fourier Transformed Infrared Spectroscopy (Nicolet
iN10 MX, Thermo, USA). The spectra were directly recorded without
any transformation or post-processing (Fig. S4).
2.3. Weight loss measurement during degradation
To assess the degradation process, the weight loss of test plastics is
widely applied in degradation tests. Here the plastic mass was weighed
and recorded before degradation on a precision balance (BSA124S,
Sartorius, Germany). Then the plastic pieces were carefully placed into
aluminum foil chambers for degradation. At each sampling time, the
surface atmospheric deposited dust or soil was slightly removed by clean
tweezers as much as possible. Then, the plastic mass was re-weighed to
obtain the weight loss values.
2.4. Microplastics separation and quantification
After six months of degradation either in the air or in soil, the
remaining PPDO debris (most of them are microplastics (plastic parti­
cles< 5 mm) was carefully collected from aluminum foils. For the
samples collected from the air environment, we gently opened the foils
and slowly transferred the remaining plastic materials into glass petri
dishes. The fragments and particles were observed and photographed
under the Zeiss microscope. The numbers of microplastics were counted
one by one manually (the lowest size limit is 50 µm) and subtracted the
J. Liao and Q. Chen
Fig. 1. Records of (a) temperature, (b) humidity, and (c) rainfall content during the whole degradation period, and (d) the sketch of experimental layout with
aluminum trays.
fibrous/particulate items from atmospheric deposition in the parallel
procedural control chambers. For the samples from the soil environ­
ment, we first gently removed the surficial soils on plastics and then
transferred them to clean 2-L glass flasks of 30 cm depth with 1 L of
saturated NaCl solution (36%, w/w) slowly for density flotation, which
can efficiently separate lighter microplastics from heavier soil particles
(He et al., 2018). The saline solution was stirred and settled for 4 h, to
minimize the potential degradation loss caused by soaking in water. The
supernatant without any soil was filtered through the 20-μm nylon filter
membranes (Millipore, USA). Then the microplastic numbers in each
sample were observed, measured, and counted similar to that in the air.
To further verify whether the particles separated from air or soil
samples were microplastics, we randomly selected around one-fourth of
particles per sample to identify their composition by a Raman micro­
scope (DXR2, Thermo Scientific, Germany). The detection rate of PPDO
is 100% in the air samples and 93% in the soil samples.
2.5. Surface morphology observation
The surface morphology of plastics before and after degradation in
either air or soil environment was examined using a Scanning Electronic
Microscope (SEM, S-4800, HITACHI, Japan). The SEM was equipped
with an accelerating voltage of 5 kV under a high vacuum. The plastic
fragments were fixed on stubs using carbon tape and sputtered with
gold: palladium (80:20) before observation.
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Journal of Hazardous Materials 418 (2021) 126329
2.6. Microorganisms collection and illumina MiSeq sequencing
An extra set of samples for microorganisms analysis in the soil
environment were also buried at the beginning of the experiment. We
collected this set of BP debris from the soil after 6-month degradation,
removed the soil adhering to the plastic surface, and then placed it into
50 mL of Milli-Q in glass beakers with 20 min ultrasonication to shake
down the biofilms. The biofilms were collected by filtering onto 0.22 µm
acetate membranes (Shanghai Xinya Co., China), and immediately
transferred to sterile centrifuge tubes for further analysis. Biofilms and
soil samples were then frozen at − 80 ◦ C. DNA extraction was performed
with the soil DNA extraction kit (Omega Bio-Tek, USA). The bacterial
16S rRNA hypervariable V3-V4 region was amplified with primers of
338F and 806R of (5’-ACTCCTACGGGAGGCAGCAG-3’) and (5’-GGAC­
TACHVGGGTWTCTAAT-3’), respectively. PCR reactions were per­
formed in triplicate of 20 μL mixture containing 2 μL of 4 μL of 5x
FastPfu buffer, 2.5 mM dNTPs, 0.8 μL of each primer (5 μM), 0.4 μL of
FastPfu polymerase, and 10 ng template DNA.
The amplicons were purified using the AxyPrep DNA Gel Extraction
Kit (Axygen Biosciences, USA) and quantified by a QuantiFluor-ST
(Promega, USA) per manufacturer’s instructions. Then, purified ampli­
cons were combined in equimolar (11 ng DNA/sample) and paired-end
sequenced (2 × 300) on a MiSeq platform (Illumina, USA) according to
the standard protocols of Majorbio Biopharm (Shanghai, China)(Li et al.,
2018).
J. Liao and Q. Chen Journal of Hazardous Materials 418 (2021) 126329

2.7. Microbial diversity analysis
After filtering, an average of 53 336 reads per sample was obtained
(min: 38 927; max: 67 351). The length distribution was 203–506 bp,
with an average length of 417 bp (Fig. S5). All samples were rarefied to
38 927 reads. Operational taxonomic units (OTUs) were clustered with a
97% similarity cutoff with UPARSE ver 7.1 (Edgar, 2013). The chimeric
sequences were identified and removed with UCHIME (Edgar et al.,
2011). Bacterial taxonomy was assigned to the species level using the
SILVA 16S rRNA database (SSU115) with a 70% confidence threshold
(Li et al., 2018).
Alfa-diversity (i.e., Sobs, Shannon, Simpson, ACE, and Chao1) was
measured from the rarefied OUT database (Table S3), and β-diversity
was estimated based on unweighted UniFrac distances analyses and
visualized by principal coordinate analysis (PCoA). Analysis of similar­
ities (ANOSIM) was performed to determine the differences among

Fig. 2. Weight loss kinetics of different plastics during six-month degradation in the air and soil environment after 6 months. The bars with blue circle dots represent
plastic weight loss values in the air, and the bars with red square dots represent plastic weight loss values in the soil. The asterisks on the top of adjacent two bars
mean the weight loss percentages for plastics between air and soil environment were significantly different (p < 0.05). (a) PPDO: poly(p-dioxanone); (b) PLA: poly
(lactic acid); (c) PBAT: poly(butylene adipate-co-terephthalate); (d) PLA blend: 50% of PLA+ 50% polyethylene; (e) PBAT blend: 90% PBAT+ 10% PLA; (f) MD40:
40% mineral doped polyethylene. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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J. Liao and Q. Chen Journal of Hazardous Materials 418 (2021) 126329

groups with Bray- Curtis as similarity index (Clarke, 1993). A heatmap
of the log2 transformed counts of the top 50 taxa with the largest overall
variance was generated from the relative abundance of OTUs.
2.8. Data analysis and statistics
Microbial diversity diagrams were produced using R packages (ver
2.15). Multiple hypothesis tests were adjusted using Benjamini and
Hochberg’s false discovery rate (FDR) with a threshold of 0.05 (Tang
et al., 2018). Differences between the air and soil degradation were
tested by the t-test, and differences among microplastic size groups were
tested by the one-way ANOVA, and the significant level for all analyses
was set when p < 0.05 (SPSS, ver 22).
3. Results
3.1. Degradation levels of biodegradable plastics in the natural
environment
Due to the lack of abundant microorganisms, photodegradation was
dominant for the plastic degradation in the air. Compared with the non-
biodegradable PE plastic (1.3 ± 4.0% weight loss after 6 months)
(Fig. S6), only PPDO showed an obvious degradation level after 1.5-
month incubation and reached 54.7 ± 9.1% weight loss after 6-month
degradation (Fig. 2a). The degradation levels for PLA, PBAT, PLA_­
blend, PBAT_blend, and MD40 were 1.1 ± 0.4%, 0.8 ± 0.2%,
− 1.5 ± 0.3%, − 0.3 ± 0.1%, and − 0.8 ± 0.1%, respectively (Fig. 2b–f).
The plastic surface would be covered with biofilms, dust, and soil
after exposure to the natural environment. The surface dust, biofilms, or
soil were gently removed by clean tweezers as much as possible before
the plastic weight measurement. It is difficult to remove the biofilms/
dust completely because some of the biofilms and dust were associated
tightly with plastics, and the plastic would be broken if they were
cleaned hard. As for easily degradable plastics, the weight of biofilms
and remaining dust is negligible. But for the not easily degradable
plastics, when the biofilms and dust weight was greater than the weight
loss due to plastic degradation, the weight loss value was negative.
Biodegradation takes a dominant place when plastics were incubated
in the soil. Compared with the non-biodegradable PE plastic
(− 0.1 ± 0.3% weight loss) (Fig. S6), only three kinds of plastics have
more than 5% of the original plastic weight degraded, with weight loss
of 56.8 ± 4.8% for PPDO, 8.0 ± 0.0% for PLA, and 6.8 ± 0.3% for PBAT
(Fig. 2a–c), and the degradation level of MD40 was almost negligible
(0.7 ± 0.2%) (Fig. 2f). For PLA and PBAT blends, the plastic weights

Fig. 3. Surface morphology characteristics of plastics with relatively good degradability in their original state, after 6-month degradation in the air, and after 6-
month degradation in the soil. (a-c) PPDO; (d-f) PLA; (g-i) PBAT. PPDO: poly(p-dioxanone); PLA: poly(lactic acid); PBAT: poly(butylene adipate-co-tere­
phthalate). The yellow arrows indicate the formation of plastic cracks and fragments, the red arrow indicates crystalline squares appeared on the PPDO plastic
surface, and the green arrows indicate the formation of microplastics. (For interpretation of the references to colour in this figure legend, the reader is referred to the
web version of this article.)

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J. Liao and Q. Chen
were even increased in the soil, with 1.7 ± 1.0% and − 0.3 ± 0.1% for
PBAT_blend and PLA_blend, respectively (Fig. 2d and e), which was
mainly because that the weight of biofilms closely bound on the plastic
surface was heavier than that of degradation loss.
Sophisticated characteristics of the plastic surfaces were observed
using scanning electron microscopy (SEM). The surface of the original
plastics (PPDO, PLA, and PBAT) was relatively smooth (Fig. 3a, d, g).
However, the roughening of surfaces (Fig. 3b and c, e and f, h and i), and
formation of cracks and fragments (Fig. 3c, e, f, h, i, indicated by yellow
arrows) were observed under both air or soil environment for these three
kinds of plastics which exhibited obvious degradation phenomenon
(Fig. 2).
For the PPDO, even crystalline squares appeared on the surface
(Fig. 3b, indicated by a red arrow). The formation of microplastics can
also be observed under SEM, especially on the plastics degraded in the
soil, which can be deemed as an indication of microbial attack (Fig. 3b,
c, f, i, indicated by green arrows). The surface of PLA_blend, PBAT_­
blend, MD40, and PE were also weathered to some extent, albeit not
obvious (Fig. S7).
3.2. Microplastics released after degradation
Even though PPDO had the highest weight loss, there were still
numerous remains of PPDO microplastics in either air or soil environ­
ment after degradation, which was verified by the Raman spectrum
(Fig. 4). The abundance of microplastics formed by degradation in the
soil (2103 ± 131 item/g original plastic) was significantly higher than
that in the air (441 ± 326 item/g original plastic) (p < 0.05) (Fig. 5a).
The particle size distribution of microplastics after degradation in the air
mainly fell into the range of 50–500 µm, and particle abundance
decreased with the increase of particle size (Fig. 5b); microplastics
formed in the soil mostly fell into the range of 50–500 µm, and a high
portion of microplastics were also found within 500-5000 µm range
(Fig. 5c).
3.3. Plastic degradation relates to microbial composition
We further analyzed the microbial composition on different plastics
collected from the soil environment after 6-month degradation.
Fig. 4. Identification of PPDO microplastics formed in the air and soil environment. (a) microplastics formed in the air environment; (b) the surface morphology of a
microplastic from the figure a; (c) the Raman spectrum of the microplastics in the figure b; (d) microplastics formed in the soil environment; (e) the surface
morphology of a microplastic from the figure d; (f) the spectrum of the microplastics in the figure e.
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Journal of Hazardous Materials 418 (2021) 126329
According to the Venn analysis result, PPDO had the richest microbial
species of 3 528 OTUs detected, with 922 (18.84%) distinct OTUs from
other plastics (Fig. 6a). Moreover, the Circos analysis indicated that the
phylum taxa diversity follows the order of PPDO, PLA, PBAT, and other
plastics (Fig. 6b). The above results suggest that the biodegradation
levels in the soil are probably highly related to the diversity and richness
of microorganisms on plastics.
For more details, microbial community profiles at the genus level
were demonstrated by a hierarchically clustered heatmap (Fig. 6c). The
top 50 classified genera and 7 samples were both hierarchically clus­
tered based on the Bray-Curtis similarity index. It indicated that the soil
and PPDO were the most similar samples, and we marked these two as
Group I in the figure; other plastics were marked as Group II (Fig. 6c).
Through the dimension reduction analysis of PCoA, different plastic and
soil samples were well grouped (R= 0.93, p = 0.001). It was demon­
strated that microbial diversity was the largest separation factor
(PCoA1), accounting for 29.45%, and the second separation factor
(PCoA2) related to degradability, accounting for 21.55% (Fig. 6d).
It is worth noting that although the microbial species data were
normally distributed and homogenous on all biofilms collected from
different plastics, the microbiota on PPDO was visually different from
other plastics according to the LEfSe analysis (Fig. 6e). Other plastic had
higher proportions of Patescibacteria than that of PPDO
(1.084 ± 0.404% in PPDO, 13.21 ± 9.84% in other plastics). But most of
the other taxa were significantly richer in the group of PPDO. For
instance, Chloroflexi (7.239 ± 4.61% in PPDO, 1.039 ± 0.6814% in
other plastics) and Firmicutes (7.609 ± 5.47% in PPDO,
0.3251 ± 0.3008% in other plastics) were higher in PPDO.
4. Discussion
4.1. Degradation mechanisms under different environmental conditions
Our results found that PPDO, PLA, and PBAT can degrade under
environmental conditions, but the degradation levels are slower
compared to the requirements of the standard degradation tests under
composting conditions (i.e. 90% degradation levels after 3 months) (ISO
17556, 2019; ISO 22404, 2019). This is because the relatively high
temperature and moisture conditions in compost environment are not
J. Liao and Q. Chen
Fig. 5. Microplastics released from PPDO biodegradable plastics after six-month degradation in the air and soil environment. (a) microplastic particle abundance; (b)
microplastic size distribution after degradation in the air; (c) microplastic size distribution after degradation in the soil. Microplastic abundance was expressed as
formed microplastic particle number per original plastic mass. * represents the microplastic concentrations have significant differences between the air and soil
environment (p < 0.05). Different lowercase letters on the bars represent significant differences among them (p < 0.05).
always reliable under natural conditions The degradation performance
of PPDO was the best with around 60%; however, lower than 10% was
achieved for PLA and PBAT in the air and soil (Fig. 2). The action of
microbial communities, together with a variety of mechanisms such as
UV radiation, photo-oxidation, physical heating/cooling, and hydrolysis
were responsible for the fragmentation of BPs (Klein et al., 2018; Lucas
et al., 2008).
When BPs were exposed to the air environment, photodegradation is
the most important degradation mechanism. BPs are susceptible to
degradation initiated by natural light, especially the lights in the near-
UV bands of 290–400 nm. The photons can carry the energy and
create unstable states in the polymer macromolecules and even cleave
C‒C bonds (Lucas et al., 2008). The BPs’ photodegradation can be
depicted by Norrish reactions consisting of photoionization and chain
scission stages (Nakamura et al., 2006), and crosslinking reactions, or
oxidative processes (Lucas et al., 2008). For instance, the photo­
degradation of PLA can be described by the Norrish reaction (Tsuji et al.,
2006), and the crosslinking reactions are mainly responsible for the
brittleness of PBAT (Kijchavengkul et al., 2008). Additionally, photo­
degradation can also lead to the reduction in molecular weight and the
loss of mechanical properties of BPs (Singh and Sharma, 2008).
When BPs were exposed to the soil environment, biodegradation was
the most important degradation mechanism, as the soil was rich in mi­
croorganisms. Biodegradation is mainly driven by microorganisms,
which can secrete certain catalytic agents to cleave polymeric molecules
and produce new biomass and metabolites by several steps including
microorganisms biofilm formation, polymer assimilation, plastic frag­
mentation, and metabolites and gas molecules releasing (Shabina et al.,
2015; Bano et al., 2017; Arutchelvi et al., 2008; Bhardwaj et al., 2012).
Among the biodegradation, the assimilation step is important. All BPs
have hydrolytic bonds, and the hydrolysis reactions need hydrolase
enzymes to catalyze (Bano et al., 2017). Thus, enzymes play a major role
in the microbial degradation of BPs. For instance, microorganisms with
PLA degradation ability can secrete corresponding extracellular depo­
lymerase (Wang et al., 2011), which is stimulated by inducers such as
silk fibroin, elastin, and gelatin, to accelerate biodegradation.
In this study, we did not adopt standard testing conditions, therefore
the obtained results may have the following limitations. (1) The
degradation levels of these plastics can only reflect their performance in
a typical subtropical environment of warm seasons (from May to
November). (2) The utilization of aluminum trays may limit the contact
between the samples and the soil by restricting the migration of soil
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Journal of Hazardous Materials 418 (2021) 126329
microorganisms. From this perspective, the degradation level may be
underestimated to some extent. (3) As we attempted to highlight the
degradation performance of BPs between natural and standard test en­
vironments, we did not include positive control in this study which is
similar to that of the standards (i.e., ISO 17556/16929 (ISO 17556,
2019; ISO 16929, 2019)). However, positive controls (e.g. cotton, other
natural fabrics, or materials known to bio-integrate) would be helpful
for degradation performance comparison with easily degradable mate­
rials, which need to be included in future studies.
Collectively, the degradation levels were slow under natural air and
soil environmental conditions. In our opinion, it was probably due to the
temperature and humidity did not meet the optimum growth conditions
for microorganisms. If the degradation levels of most BPs are not
significantly different from that of non-biodegradable plastics in the
natural environment, the limited advantages of BPs will benefit the
environment once they are released into the natural environment, which
issue is the BP industry claims to solve.
4.2. Different plastics exhibited distinct degradation patterns
The majority of BPs tested in the present study failed to achieve the
lowest 60% degradation level according to BP degradation standards
(Kjeldsen et al., 2018), except for PPDO with 44.3–61.3% in the air and
51.7–61.4% in the soil after 6-month degradation. Generally speaking,
the degradation level followed the order of pure BPs> BP blends> ­
claimed “BP”≈ non-biodegradable plastic (polyethylene).
Apart from biotic and abiotic factors in the natural environment, the
architecture of polymers can affect the degradation level, including
molecular weight and distribution (Sun et al., 2010), the type of polymer
chain structures (Park et al., 2010; Li et al., 2006), etc. The molecular
weight of PPDO, PLA, and PBAT are basically of the same order of
magnitude, and all of them are of linear chain structure; however, PPDO
exhibited more excellent degradation performance even in the air
(Fig. 2). This is because PPDO had a better affinity with water molecules
because of its special ether bond (Wu et al., 2015), and thus a good
degradation performance of PPDO was still achieved in the air under the
humidity of 76% and temperature 25 ◦ C on average (Fig. 1a and b). In
the soil environment, PPDO also showed the best degradation perfor­
mance, which is mainly due to the more diverse and abundant micro­
organisms on the biofilms of PPDO, which will be discussed in detail in
Discussion 4.4.
A huge variety of BP blends have been investigated in the past decade
J. Liao and Q. Chen Journal of Hazardous Materials 418 (2021) 126329

(caption on next page)

8
J. Liao and Q. Chen Journal of Hazardous Materials 418 (2021) 126329

Fig. 6. Microbial community composition analysis of different plastics collected from the soil environment after 6-month degradation. (a) Venn diagram of OUT
distribution, which shows the number of different and shared OTUs among plastic groups; (b) Circos analysis, which reflects the abundance of different phyla in
plastic biofilms with different colors of each side of the connecting bands between the sample groups and microorganism compositions; (c) Hierarchically clustered
heatmap, which shows distribution pattern of microorganisms on plastics and soil at the genus level; (d) PCoA analysis, which helps us to visualize the differences
among groups by clustering microorganisms on beta diversity; (e) LEfSe analysis with Wilcoxon rank-sum test (only significant results showed). Circles radiated from
inside to outside in the figure represent the classification level from phylum to genus. Each small circle at a different classification level represents a classification at
that level, and the diameter of the small circle represents the relative abundance. The species with no significant differences are uniformly colored in yellow, while
the species with significant differences are colored according to the group. PPDO: poly(p-dioxanone); PLA: poly(lactic acid); PBAT: poly(butylene adipate-co-tere­
phthalate); PBAT blend: 90% PBAT+ 10% PLA; PLA blend: 50% of PLA+ 50% PE; MD40: 40% mineral doped PE; PE: polyethylene. (For interpretation of the
references to colour in this figure legend, the reader is referred to the web version of this article.)

to introduce new functionality to BPs, and scientists are particularly
interested in PLA due to its advantages of natural origin and biode­
gradability and disadvantage of brittleness (Narancic et al., 2018;
Lovinčić Milovanović et al., 2019). For instance, the poor mechanical
and physical properties of PLA can be blended with other plastics to
conquer its brittleness (Ploypetchara et al., 2014; Yao et al., 2011). In
the present study, we found that both PLA blend (with PE) and PBAT
blend (with PLA) showed worse degradation performance than their
respective pure BPs, which may be due to the improved mechanical
properties after blending (Narancic et al., 2018). The promoted me­
chanical properties of polymers caused it difficult to fragment or crack
into small pieces. Besides, previous research also showed that plastic
surface hydrophobicity can be significantly modified on PLA blend (with
PE) (Vrsaljko et al., 2016; Thurber et al., 2015). Consequently, the hy­
drolysis reaction by microorganisms becomes more difficult than before,
and the degradation level is thus reduced.
The MD40, which claims to be a “BP”, showed almost no signs of
biodegradation compared with non-biodegradable PE. This is because
MD40 is a 40% mineral doped PE plastic. It may be even more difficult to
degrade than PE. Therefore, due to the chaotic BP sales market, it is
highly recommended to strengthen supervision and avoid the phenom­
enon of false advertising.
4.3. Formation of microplastics during degradation
The principle of BP degradation is to reduce the difficulty of long-
chain cleavage, and the degradation process involves deterioration,
fragmentation, and finally bioassimilation (Shen et al., 2020; Emadian
et al., 2017). Small fragments of plastics, oligomers, and monomers can
present in the environment before BPs’ complete degradation. These
crystalline square fragments (Fig. 3b) were probably due to the initial
degradation of the amorphous fraction of PPDO, which will finally lead
to slower-degrading crystalline parts out of the material (Shah et al.,
2008). This is one of the reasons why numerous remaining microplastics
were found after 6-month degradation (Figs. 4–5). Additionally, the
enzymatic hydrolysis efficiency of BPs depends on the ratio L and D
forms of polymers. As most natural enzymes are D specific, they cannot
degrade L-monomers and thus, resulting in the L-forms of microplastics
(Shen et al., 2020). Moreover, the crystalline region percentages of BPs
also affect the formation of microplastics. For instance, as a semi­
crystalline polymer, the chains of PPDO in amorphous regions can be
quickly hydrolyzed; however, the crystalline regions can form crystal­
line residues (Fig. 3b) after the disappearance of amorphous regions,
which is known as a ‘‘cleavage induced crystallization process’’ (Zong
et al., 1999; Chen et al., 2007).
Of note, the formation of microplastics during the degradation pro­
cess is not a special case for PPDO, because other BPs are also believed to
produce microplastics. The formation of BP microplastics degradation is
mainly due to the alteration of the physical properties of polymers
during degradation, which makes them easier to fragment. For instance,
the microbial community can degrade BPs into oligomers, dimers, and
even monomers (Shah et al., 2008; Hajighasemi et al., 2016), and
Norrish reactions in photodegradation can cause brittleness of BPs, with
could reduce BPs’ molecular weight and mechanical properties (Kij­
chavengkul et al., 2008; Singh and Sharma, 2008).
The physical properties of these BP microplastics are different from
those of non-biodegradable plastics, because BP microplastics are more
easily broken as many bonds break during degradation. Some studies
have found that the effects of BP microplastics may be different from
that of non-biodegradable microplastics. For instance, biodegradable
polyhydroxy butyrate (PHB) exhibited relative slighter effects on the
assimilation efficiency of freshwater invertebrate Gammarus fossarum
than the non-biodegradable polymethylmethacrylate microplastics
(Straub et al., 2017). But, the overall biological effect differences be­
tween BP and non-biodegradable microplastics were small (Shruti and
Kutralam-Muniasamy, 2019; González-Pleiter et al., 2019; Straub et al.,
2017). Consequently, the BP microplastics may also pose threats to the
environment. Thus, if BPs are disposed of in an uncontrolled fashion into
the natural environment, or if we cannot ensure their complete degra­
dation within a reasonable period, the accumulation of microplastics
produced by BPs would exist.
4.4. Microorganisms diversity is vital for BP degradation
PPDO has the highest degradation level in the soil, which is closely
related to the diverse and abundant microbial community on its biofilm
(Fig. 6a and b). Compared with other plastics, the microbial community
on PPDO was more similar to the microbial groups in the soil (Fig. 6c).
The β-diversity analyses also indicated significant differences between
PPDO and other plastic groups (Fig. 6d). These results were further
supported by the LEfSe analysis. Although Proteobacteria (41.21% and
55.41%) and Actinobacteriota (21.36% and 18.66%) were the two
keystone taxa for all kinds of plastics (Fig. S8), which is similar to pre­
vious studies (Gong et al., 2019; Roager and Sonnenschein, 2019; Curren
and Leong, 2019), the main differences between PPDO and other plastics
were driven primarily by the diversity and relative abundances of the
taxa of Patescibacteria, Chloroflexi, and Firmicutes (Fig. 6e).
Since Proteobacteria has been identified as a key taxon on biofilms
associated with PLA when this kind of BP was incubated in Villum and
Barba Perder soil (Ruthi et al., 2020), significantly higher abundances of
Proteobacteria on other plastics may be contributed by PLA and PLA_­
blend mainly. Firmicutes is known to be ubiquitous in the soil (Ober­
beckmann et al., 2014), and microorganisms from the phylum Firmicutes
are capable of degrading a variety of petroleum hydrocarbons (Gomes
et al., 2014; Fuentes et al., 2014). Moreover, Chloroflexi is present in
various environments, such as soil and freshwater, which is related to
carbon cycling during the reproduction phase (Sanjeeviraman, 2015;
Hug et al., 2013). As Chloroflexi and Firmicutes possessed significantly
higher abundance on PPDO biofilms than that for other plastics, it im­
plies that the microorganisms on PPDO have a stronger potential to
degrade organic materials, or PPDO provides a more suitable carbon
source for these microorganisms to grow.
4.5. Environmental significance
It should be kept in mind that the standards were developed to
specify plastics suitable to composting i.e. a biological waste treatment.
BPs are suitable to be made into disposable single-use plastics (e.g., for
packaging, straws) that should be biodegradable in a shorter time frame,
but the degradation levels (<60%) are far beyond their performance

9
J. Liao and Q. Chen
under standard environment tests, especially when they are disposed of
in an uncontrolled manner into the natural environment. Besides, some
other plastics (e.g., for phones, cars, and fishlines) are not suitable to be
made of BPs, as they should be able to be used for long periods.
Therefore, although the concept of BP is attractive, we must be careful
about the utilization and management of BPs.
The current international standards for BP biodegradation tests are
mostly carried out under composting conditions, e.g. ISO16929 (ISO
16929, 2019). The results obtained with these tests are not directly
applicable to natural environments, where conditions are different. As
the degradation level of BPs is often accelerated in the compost envi­
ronment with high temperature, high moisture, or abundant microor­
ganisms (Kjeldsen et al., 2018; Besseling et al., 2019; Liu et al., 2019),
the degradation level of BPs becomes relatively lower in the natural
environment. Then, it is necessary to have effective measures of BPs
collection and separation. Due to the chaotic collection system of con­
ventional plastics and BPs, the efficient separation of BPs seems difficult
at the moment. The coding mechanism for BP materials may be a
feasible method (Shen et al., 2020), which will largely help with the BPs
separation from other recyclable materials, and prevent BPs from com­
busted or landfilled together with conventional non-biodegradable
plastics. Otherwise, the verification of BPs’ good biodegradation per­
formance in the natural environment would be one of the most impor­
tant prerequisites before their usage.
Further, the ISO or ASTM standards pay attention solely to the
degradation levels of BPs but lack toxicity evaluation, nor potential
adverse effects to the environment during degradation. Microplastics
will be produced before the complete disappearance of BPs. Thus, it is
recommended to promote toxicity tests about BP microplastics on
environmental organisms, and other environmental risk evaluation
studies, such as the effects of BP degradation intermediates and addi­
tives to organisms during and after BP degradation.
Collectively, we need to preserve caution in the effort of promoting
BP application. It is risky to promote large-scale production and appli­
cation of BPs if the knowledge gap about their environmental effects has
not been addressed or collection and separation systems for BP disposal
systems are not sound enough.
CRediT authorship contribution statement
Jin Liao: Conceptualization, Visualization, Investigation, Software,
Writing - original draft. Qiqing Chen: Supervision, Investigation, Soft­
ware, Methodology, Writing - review & editing.
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
Special thanks to Professor Yu-zhong Wang and Professor Gang Wu
from Collaborative Innovation Center for Eco-Friendly and Fire-Safety
Polymeric Materials (MoE), State Key Laboratory of Polymer Materials
Engineering, and National Engineering Laboratory of Eco-Friendly
Polymeric Materials (Sichuan), College of Chemistry, Sichuan Univer­
sity, China. They kindly synthesized and provided PPDO plastics for
research in this study. The present study was financially supported by
the National Natural Science Foundation of China (42077371) and
(U19A2095).
Appendix A. Supporting information
Supplementary data associated with this article can be found in the
online version at doi:10.1016/j.jhazmat.2021.126329.
10
Journal of Hazardous Materials 418 (2021) 126329
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