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Biofilms Enhance the Adsorption of Toxic Contaminants on Plastic

Microfibers under Environmentally Relevant Conditions
Geetika Bhagwat, Thi Kim Anh Tran, Dane Lamb, Kala Senathirajah, Ian Grainge, Wayne O’Connor,
Albert Juhasz, and Thava Palanisami*
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ABSTRACT: Microplastics (MPs) exposed to the natural environment

provide an ideal surface for biofilm formation, which potentially acts as a
Downloaded via UNIV FED DA BAHIA on January 10, 2023 at 13:02:03 (UTC).

reactive phase facilitating the sorption of hazardous contaminants. Until now,

changes in the contaminant sorption capacity of MPs due to biofilm formation
have not been quantified. This is the first study that compared the capacity of
naturally aged, biofilm-covered microplastic fibers (BMFs) to adsorb
perfluorooctane sulfonate (PFOS) and lead (Pb) at environmentally relevant
concentrations. Changes in the surface properties and morphology of aged
microplastic fibers (MF) were studied by surface area analysis, infrared
spectroscopy, and scanning electron microscopy. Results revealed that aged
MFs exhibited higher surface areas because of biomass accumulation
compared to virgin samples and followed the order polypropylene>polyethy-
lene>nylon>polyester. The concentrations of adsorbed Pb and PFOS were 4−
25% and 20−85% higher in aged MFs and varied among the polymer types.
The increased contaminant adsorption was linked with the altered surface area and the hydrophobic/hydrophilic characteristics of
the samples. Overall, the present study demonstrates that biofilms play a decisive role in contaminant-plastic interactions and
significantly enhance the vector potential of MFs for toxic environmental contaminants. We anticipate that knowledge generated
from this study will help refine the planetary risk assessment of MPs.
KEYWORDS: lead, perfluoroalkyl substances, polyethylene, polyester, nylon, polypropylene, adsorption, isotherm

1. INTRODUCTION addition, the extracellular polymer substances (EPS), lipid

Plastics can persist for tens to thousands of years in the membranes, and apolar groups19 in biofilms can act as reactive
environment1 and are subjected to weathering factors such as phases and facilitate the adsorption of metals,20 antibiotics,21,22
and organic contaminants.23,24
ultraviolet radiation, physical abrasion, chemical oxidation, and
Several processes governing biofilm−metal interactions have
biodegradation.2 These factors promote their fragmentation,
been described in the literature. For instance, the process of
thereby generating microplastics (MPs; <5 mm).3 Recent
“biosorption” has been described as the physical immobiliza-
studies have shown that weathered plastics can accumulate
tion of aqueous metals by biologically derived sorbents for
high concentrations of organic and inorganic contaminants,
metal removal.25,26 Here, biosorption leads to the physical
including metals, 4,5 polycyclic aromatic hydrocarbons
adsorption of metals to biomass and is independent of any
(PAHs) 6−9 and per- and polyfluoroalkyl substances
metabolic reactions.27 Alternatively, the decrease in surface
(PFAS).10,11 These contaminants may exert negative impacts
hydrophobicity due to biofilms enhances the formation of
on marine biota12,13 indicating that the effects of MPs are
hydrous oxides that can scavenge metals.28 Furthermore,
associated not only with the consequences of their direct
biofilms can potentially block UV light and reduce the extent
ingestion14 but also with the potential release of chemicals
of oxidation-induced weathering, which can limit the sorption
bound to MP surfaces.15
of metals directly onto weathered plastic surfaces.29 A study on
Plastics exposed to the natural environment are readily
colonized by microorganisms capable of forming biofilms.16
Microbial biomass associated with plastics in the environment Received: March 28, 2021
can be around 6% of the total mass of plastic debris, which is Revised: June 8, 2021
highly significant considering that more than 269,000 tons of Accepted: June 9, 2021
plastics are currently residing in the world’s oceans.17 Published: June 21, 2021
Microbial colonization of plastics can influence the surface
hydrophobicity, topography, and crystallinity of plastics.18 In

© 2021 American Chemical Society https://doi.org/10.1021/acs.est.1c02012

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low-density polyethylene (LDPE) and polylactic acid (PLA) clean glass jars, and transported on ice to the laboratory. The
MP pellets incubated in an estuary indicated that metal three strands of the ropes were untwisted and rinsed again in
accumulation on MPs was directly linked to biofilm natural seawater from the pond to remove any material caught
accumulation.20 Another study showed that biofilms alter the between the strands. To exclude obvious abnormalities in
adsorption kinetics of trace metals on polystyrene (PS) terms of biofouling, attached ascidians, macroalgae, small
particles.30 Similarly, biofilms can potentially change the barnacles, and larger organic/inorganic precipitates were
adsorption properties of polyethylene (PE) MPs and enhance removed using clean forceps. The ropes were then air-dried
the role of MPs in copper tetracycline migration.31 Also, the for 30 min under a fume hood and cut into about 2−3 mm
ecotoxicity of biofilm-covered MPs spiked with silver was long pieces that instantly split further into MFs. The MFs were
found to be higher compared to that of their virgin then gently rinsed again and dried for an hour to remove
counterparts. 32 Another recent study that investigated excess water in the laminar flow and kept sealed at 4 °C until
polystyrene-associated biofilms for their Pb adsorption further analysis. As a negative control for biofouling in the
potential and combined toxicity to Daphnia magna indicated marine environment, samples of each of the polymer ropes
that biofilms intensified the vector role of MPs in the migration were incubated for the same duration in autoclaved artificial
of heavy metals in freshwater and enhanced their combined seawater prepared using sea salt (Instant Ocean, Virginia,
toxicity.33 USA). The sterilized seawater was periodically changed to
Perfluorooctanesulfonic acid (PFOS) is a chemical that avoid any unexpected microbial growth over time. The virgin
belongs to the family of polyfluoroalkyl substances and is MFs (VMFs) for the adsorption experiment were prepared
known to be highly hazardous due to contaminants which using the same methods mentioned above. Water from the
belong to the family of polyfluoroalkyl substances which are aging pond was subjected to a two-stage sterilization process
known to be disastrous in their global distribution,34,35 (1-micron filters followed by the ozone treatment) and used
toxicity,36 bioaccumulation,37−39 environmental persistence, for adsorption experiments described in Section 2.5.
and long-range transport potential. However, only a few 2.3. Sample Characterization. VMFs and biofilm-
studies have investigated the interactions between PFOS, covered MFs (BMFs) were first completely air-dried and
biofilms, and plastic materials. The bioconcentration of PFAS then characterized by attenuated total reflection Fourier
in periphytic biofilms was found to be inversely proportional to transform infrared spectroscopy (ATR-FTIR) in the absorb-
the dissolved PFOS levels, indicating concentration-dependent ance mode (see Supporting Information-M1 for more details).
bioaccumulation in biofilms.40 A recent study indicated high The Brunauer−Emmett−Teller (BET) surface areas were
accumulation of metals, PAHs, and PFAS in plastic-associated calculated for each type of sample from nitrogen physisorption
organic and inorganic matter.41 Another study reported higher data at 77 K after degassing the samples at 298 K using a
adsorption of PFAS on real environmental plastics because of surface area and porosity analyzer (ASAP 2420, Micromeritics
the presence of natural organic matter.11 Likewise, contami- Instrument Corp., USA). The surface morphology of the MPs
nant adsorption characteristics of biofilms were also used in was inspected by scanning electron microscopy (SEM), and
remediation applications, for instance, biochar with active the elemental composition of biofilms and associate precip-
biofilms was reported to efficiently remove PFAS in an on-site itates was assessed by energy dispersive spectroscopy (EDS)
wastewater treatment system.42 Despite accumulating evidence (Supporting Information-M2). Biofilm biomass was quantified
of several biofilm-mediated processes, current literature lacks using a modified crystal violet (CV) method45 for samples
information on the role of biofilms in contaminant sorption by collected at 13- and 26-week incubation (Supporting
MPs and warrants detailed investigation. To begin addressing Information-M3). The weight of biofilms attached to each
the knowledge gap, the influence of biofilms on the sorption sample was also determined per unit weight of the ropes
capacity of microplastic fibers (MFs) was investigated using a (Supporting Information-M4).
model organic (PFOS) and inorganic contaminant (Pb). MFs 2.4. Baseline Concentrations of Contaminants. Base-
were used as model MPs as they are commonly found in the line concentrations of Pb and PFOS in sterile water from the
marine environment and toxicologically relevant. We hypothe- aging pond and in the VMFs and BMFs were determined using
sized that the presence of biofilms on MFs would influence inductively coupled plasma-mass spectroscopy (ICP-MS),
their capacity to sorb Pb and PFOS under environmentally described in Supporting Information-M5, and liquid chroma-
relevant conditions and concentrations. tography coupled to tandem mass spectrometry (LC−MS/
MS), described in Supporting Information-M6. Environmental
2. MATERIALS AND METHODS metadata such as temperature, pH, dissolved organic carbon,
2.1. In Situ Weathering. We obtained three-strand PE, dissolved oxygen, salinity, and redox potential were measured
polypropylene (PP), polyester (PES) and nylon (PA) ropes of on-site (Supporting Information-M7). The baseline concen-
6 mm diameter, made to Australian standard AS4142.2−1993 tration of Pb in sterile seawater (pH = 7.9) used for adsorption
from a local supplier (The Boat Warehouse, Belrose, NSW, experiments was 0.15 μg·L−1 and below the detection limit for
Australia). These polymer types were chosen because of their PFOS (>0.01 μg·L−1). The concentration of Pb on the
common use in consumer products, textile industries, and incubated samples (BMF) at the end of incubation was 0.21−
aquaculture operations.43,44 To induce natural environmental 0.43 μg·g−1 (see Supporting Information Table S1).
weathering and biofilm formation, ropes were submerged for 6 2.5. Adsorption Kinetics and Isotherm Experiment.
months (21.01.20−20.07.20) in a large open aquaculture pond Batch adsorption experiments were designed as follows: 354
(aging pond) located at Port Stephens Fisheries, Australia polypropylene tubes were filled with 20 mL of sterile seawater
(152°05′64.87″E, 32°74′58.16”S). The pond was periodically from the aging pond amended with 1 mg·L−1 of Pb prepared
replenished with natural seawater to maintain the water level. with Pb-acetate and 10 g·L−1 of each type of VMF and BMF.
2.2. Sample Preparation. At the end of incubation, ropes This concentration was chosen considering the solubility of Pb
were gently rinsed with water from the aging pond, placed into in seawater (1.3−1.6 mg·L −1 ) and its environmental
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relevance46 and to achieve an environmentally relevant

concentration of lead found on MPs globally.47,48 The tubes
were agitated on an orbital shaker (150 rpm at 22 ° C) with
adsorption assessed at 0, 0.16, 0.5, 1, 2, 4, 8, 12, 18, 24, 36, 48,
96, and 168 h. For batch adsorption with PFOS, 165 PP vials
were filled with 20 mL of sterile seawater amended with 20 μg·
L−1 PFOS and 5 g·L−1 of each type of VMF and BMF. The
tubes were agitated on an orbital shaker (150 rpm at 22 ° C)
with adsorption assessed at 0, 2, 3, 4, 7, 10, and 30 days. After
each time point, three blanks and three replicates of each
sample type were removed for analysis. The concentrations of
Pb and PFOS in the aqueous phase were determined by ICP-
MS and LC−MS/MS, respectively. Adsorption isotherms for Figure 1. Changes in absorbance (an indirect measure of biofilm
Pb and PFOS were conducted with the concentration ranges of biomass) of crystal violet dye overtime for four plastic materials
0.5−10 mg·L−1 Pb and 5−100 μg·L−1 PFOS using the batch immersed in a natural aging pond. Error bars represent the standard
adsorption approach as described above. deviation about the mean (n = 3).
2.6. Desorption Experiment. Because the adsorption and
desorption of contaminants frequently occur in the natural
environment, the desorption tests aimed at understanding the further suggested the presence of oxygen-containing groups
impact of biofilms on the contaminant desorption rates from commonly found in the various components of microbial
the surface of MFs under comparatively pristine conditions. biofilms. Weathering of plastic polymers is commonly
The desorption experiments were conducted following the indicated by an increase in carbon−oxygen (C−O) and/or
adsorption experiments using 0.5 g of VMF and BMF carbonyl bonds (CO). These indices were calculated as the
previously loaded with Pb and PFOS. The desorption ratio of the maximum absorbance for the C−O (numerator)
experiment followed the kinetics experiment protocol and relative to the value of the reference peaks (denominator) used
was assessed twice at 22 °C in 50 mL of sterile seawater for each sample type for data normalization. The significant
previously used in the batch adsorption experiment. increase in the C−O peak in the BMF is indicated by a gray
2.7. Data Analysis, Quality Assurance, and Quality dotted line (Figure 2). However, because the C−O and Si−O
Control. The pseudo first-order model (PFO), pseudo stretchings are observed in the same IR region, results from the
second-order model (PSO), and Elovich equation were used EDS analysis were consulted. Elemental composition deter-
to describe sorption kinetics10,49 because the kinetic behaviors mined by EDS (Supporting Information-M2) indicated that Si
of a range of sorption systems can be well described with these is the third most abundant element found in aged samples after
models (Supporting Information Table S2). Langmuir, C and O, which was likely due to the accumulation of
Freundlich, and linear isotherm equations were fitted to the inorganic matter and diatoms, as discussed in the next section
isotherm data (Supporting Information Table S2). The fitting (Figure 3). The intensity of a spectral region between 1052−
of experimental data and statistical analysis was performed 1085 cm−1 (shaded in blue) was high in all four BMFs, which
using SPSS for Mac (version 27) and Microsoft Excel at a represents ring vibrations from polysaccharides, and is used as
significance level of α = 0.05. Please refer Supporting an indicator of biofilm formation.51
Information-M8 for more details on quality assurance, Numerous studies have shown that plastic surfaces exposed
calibration, mass balance, and method recovery. to the natural marine environment accumulate biogenic
materials and are colonized by microbes that form biofilms
3. RESULTS AND DISCUSSION within a few days.17,52 A recently published study by our group
3.1. Sample Characterization. The estimation of biofilm reported the presence of functionally active biofilms within two
biomass using the CV method indicated a gradual and months of incubation in the marine environment.16 Here,
significant (6−26 times) increase in the amount of biomass biofilm formation was confirmed when BMFs were examined
at 13-week and 26-week sampling (Figure 1). The initial by SEM, which revealed biofilm and associated precipitates
binding of CV, as seen in PA-VMF samples in Figure 1, is covering the samples (Figure 3). A high concentration of
perhaps due to the highly polar amide (−CONH−) functional diatoms was consistently found on PE-BMF (Figure 3A2),
groups in PES which provide sites for hydrogen bonding to while a thick layer of biofilm was also seen on PP-BMF (Figure
ionic and polar groups (electron-donor sites) in the dye 3B2). In contrast, relatively lower amounts of biomass were
molecules. The CV binding in PES samples could be a result of seen attached to PES-BMF and PA-BMF, which could be due
the ester bond (−COO−) that may allow pi-pi interactions. to their relatively smoother surface (Figure 3C2,D2), small
The dry weights of biofilms associated with PE, PP, PES and pore diameter, and surface area compared to those of PE-BMF
PA ropes were 1.1, 1.45, 0.8, and 0.78% of the weight of the and PP-BMF (Table 1). Results were congruent with the
ropes, respectively. literature, which suggests that surface topography can
The reference peaks (*) for PE (2915 and 2848 cm−1), PP significantly influence the bacterial sensing of and attachment
(2953, 2916, and 2849 cm−1), PES (1710 cm−1), and PA to material surfaces.53 The highest increase in the surface area
(1540 and 1633 cm−1) were identified by ATR-FTIR (Figure because of biofilm formation was seen in PP-BMF, followed by
2).50 The intensity of a spectral region between 1052−1085 PE-BMF, which could be due to their hydrophobic nature.
cm−1 (shaded in blue) was high in all four BMFs, which Surface hydrophobicity is known to reduce specific repulsion
represents ring vibrations from polysaccharides, and is used as forces between the microbial cell surface and the substratum
an indicator of biofilm formation.51 The increase in oxygen in that are active within a certain distance from the substratum;
BMFs indicated by EDS results (Supporting Information-M2) hence, most investigations have found that microorganisms
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Figure 2. FTIR spectrogram of virgin and biofilm-associated (A) PE, (B) PP, (C) PES, and (D) PA MFs incubated for six months under natural
marine conditions. The reference peaks for the polymers are indicated by “*”, and the regions representing carbon−oxygen bonds are represented
by a vertical black line, which is indicative of the biofilm formation and sample weathering.

attach more rapidly to hydrophobic and nonpolar surfa- h, Pb sorption on PP-VMF and PP-BMF was 0.060 ± 0.002
ces.54−57 and 0.071 ± 0.001 mg.g−1, respectively. Both PE-BMF and PP-
3.2. Lead Adsorption. Lead adsorption data for PE-MF BMF attained quasi-equilibrium at 18−24 h and showed the
and PP-MF were best fitted to a PFO model, while PES-MF highest increase in Pb adsorption due to biofilm formation.
and PA-MF were best fitted to the PSO and Elovich models Furthermore, a higher surface area in the incubated PP-MF
(parameter values are provided in Supporting Information samples would have become available because of the frequent
Table S3). The PFO kinetic model assumes that one Pb ion is splitting of fibers allowing higher biomass accumulation, as
adsorbed onto one unoccupied site on the substrate surface,58 seen in Figure 3B2. At a contact time of 1 h, Pb adsorption on
while PSO assumes that chemical sorption governs Pb PES samples was rapid, and significant differences (p < 0.05) in
adsorption.59,60 It is also worth noting that these empirical Pb adsorption were observed in the PES-VMF (0.076 ± 0.002
models may lack a specific physical meaning while investigating mg.g−1) and PES-BMF (0.084 ± 0.003 mg.g−1) samples
the mass-transfer mechanisms as their solving methods are (Figure 4c). The fastest (84−86%) Pb adsorption was attained
complicated.61 In PA-MF, both PSO and the Elovich models in the PA-MF samples at a contact time of 1 h, which was
fitted better than the PFO model, suggesting that Pb significantly different in PA-VMF (0.082 ± 0.003 mg.g−1) and
adsorption on PA-MF was predominantly chemical inter- PA-BMF (0.084 ± 0.004 mg.g−1) (Figure 4d). Both the PES-
actions.62 In a study on aged PA MPs spiked with 8 mg·L−1 of BMF and PA-BMF samples attained quasi-equilibrium at 18 h
Pb, the mass-transfer process of Pb on aged PA was suggested and adsorbed the highest amount of Pb compared to other
to be external and intraparticle diffusion.49 Overall, the samples. This is in agreement with the literature on the
goodness of fit represented by the regression coefficient adsorption of metals on MPs.49,64−66 The overall increase in
(Supporting Information Table S3) defining the relationship adsorption due to biofilms in PES-BMF (4.28 ± 2%) and PA-
between the PSO and PFO equations was better for VMF than BMF (4.02 ± 2.2%) was nearly similar. The high innate
that for BMF. This can be attributed to Pb and biofilm-covered capacity for Pb adsorption observed in the PES and PA
surfaces not always attaining equilibrium because of greater samples could be due to the presence of oxygenated (ester and
heterogeneity and porosity in the BMF samples, as indicated in amide) groups that can combine with Pb easily to form metal
surface analysis. complexes. The hydrophilicity of these polymers also allows for
At equilibrium, the adsorption of Pb was higher on all types the enhancement of water flux and removal of Pb from
of BMF compared to VMF, as seen in Figure 4. At a contact solutions.67 Although the amount of adsorbed Pb was higher in
time of 24 h, significant (p < 0.05) differences in Pb sorption PES-MF and PA-MF than in hydrophobic PE-MF and PP-MF
on PE-VMF (0.044 ± 0.0011 mg.g−1) and PE-BMF (0.0556 ± in the present study, higher biofilm accumulation on the latter
0.001 mg.g−1) were observed (Figure 4a), and the overall two altered their capacity for Pb adsorption significantly,
increase in Pb adsorption because of biofilms in PE-BMF was highlighting the crucial role of biofilms in metal accumulation.
12.32 ± 1.9%. The highest increase in Pb adsorption among all The adsorption isotherm of Pb on VMFs and BMFs (Figure
the BMF was 20.54 ± 3.2%, as seen in PP-BMF (Figure 4b). 5) followed a Langmuir model better than a Freundlich model,
The highest surface area and porosity of PP-MF (Table 1) as indicated by the correlation coefficient values (Supporting
could have facilitated a higher accumulation of biofilms that Information Table S4). Values for equilibrium parameter RL,
present many organic, oxygen-containing functional groups calculated from the Langmuir eq (Supporting Information
such as carboxyl and aldehyde, hydroxyl sulfhydryl, phosphor- Table S5), were in the range of 0−1, indicating that the
yl, and amines to which Pb may bind.63 At a contact time of 24 adsorption process of Pb on both VMFs and BMFs was
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(provided by MFs) and pH (seawater), as previously indicated

in adsorption studies on various MPs.49,65,69 A study
conducted with aged (undetermined) PA ropes49 reported a
higher Qmax of Pb adsorption (1.03 mg.g−1 at 27 °C, pH 5)
than that of PA-BMF used in the present study (0.27 mg.g−1 at
22 °C, pH 7.9). Because the extent of aging was not stated, the
influence on the adsorption capacity could have been due to
multiple complex variables described earlier. Although studies
that investigated the impact of pH and temperature on metal
adsorption on MPs49,65 ruled out contradictory inferences,
environmental weathering and biofilm formation have been
consistently shown throughout the literature (Supporting
Information Table S6) to increase the metal adsorption
capacity of MPs.20,30,70
3.3. PFOS Adsorption. PFOS adsorption data for BMF
were well fitted equally to both PFO and PSO models, as
indicated by the determinant coefficient values (Supporting
Information Table S7), suggesting that both chemisorption
and physisorption could explain the PFOS adsorption on the
experimentally submerged and aged samples in the study. At
30 days, the adsorption of PFOS was significantly (P < 0.05)
higher on all four types of BMFs, as indicated by black triangles
in Figure 6. At a contact time of 3 days, the PE-VMF and PE-
BMF samples sorbed 1.12 ± 5.8 × 10−3 μg·g−1 and 2.02 ± 2.2
× 10−2 μg·g−1 of PFOS, respectively (Figure 6a), and the
increase in PFOS adsorption due to biofilms in the PE-BMF
samples was 75.6 ± 2.4% higher than that in PE-VMF. The
highest increase in the adsorption of PFOS due to biofilms was
seen in PP samples in which PFOS adsorption was 80 ± 7.4%
higher in PP-BMF compared to that in PP-VMF (Figure 6b).
At a contact time of 3 days, 0.79 ± 5 × 10−3 μg·g−1 and 1.58 ±
2.7 × 10−2 μg·g−1 of PFOS were sorbed on PP-VMF and PP-
BMF, respectively. The adsorption of PFOS on VMF could be
a combined result of hydrophobic and weak van der Waals
forces and the self-aggregation of PFOS. While in BMF, it is
likely that there were competitive adsorption rates between the
Figure 3. SEM images and pictures of plastic ropes weathered for six plastic surface and natural organic matter/biomass, and the
months under marine conditions: (A1) surface of PE-VMF (A2) PE- interactions were dominated by hydrophobic interactions and
BMF heavily covered with diatoms, (B1) PP-VMF, (B2) PP-BMF not cationic exchange.10,11,71
splitting into smaller fibers and covered with the thick coating of After 3 days, the PES-VMF samples reached nearly 63%
biomass, (C1) PES-VMF, (C2) PES-BMF covered with salt (1.35 ± 5 × 10−3 μg·g−1) of the adsorption capacity, while in
precipitates and diatoms, (D1) PA-VMF, and (A2) PA-BMF covered
with biomass. PES-BMF, the samples reached nearly 72% (2.09 ± 4.7 × 10−3
μg·g−1) of the adsorption capacity (Figure 6c). The total
increase in PFOS adsorption due to biofilms in 2.09 ± 4.7 ×
favorable. The maximum adsorption capacity (Qmax) for Pb 10−3 μg·g−1 was 35.12 ± 1.1%. The fastest adsorption of PFOS
adsorption when fitted to the Langmuir model in the VMF was observed in the PA-MF samples in which in 3 days, nearly
samples was 8−14.7 × 10−2 mg·g−1 compared to 10.9−27.2 × 75% (2.01 ± 2.3 × 10−3 μg·g−1) and 80% (2.59 ± 9 × 10−3 μg·
10−2 mg·g−1 in the BMF samples (Supporting Information g−1) adsorption capacities were attained in PA-VMF and PA-
Table S6). The Qmax of Pb adsorption in PE-VMF used in the BMF, respectively (Figure 6d). The overall increase in PFOS
present study (8 × 10−2 mg.g−1) was higher than the Qmax of adsorption due to biofilms in PA-MF was 20.9 ± 2.3%.
virgin PE MPs (pellets) reported previously68 (0.191 × 10−3 The total percentage uptake of PFOS among the four types
mg.g−1), which could be due to the higher surface area of polymers at the end of 30 days was highest in the PA-VMF

Table 1. Material Properties of MFs Used in This Study

adsorption pore
BET surface area (m2 g−1) diameter (nm)
polymer VMF BMF average increase in surface area due to biofilms specific gravity (gcm−3) VMF BMF
PE 0.3818 ± 0.06 0.6469 ± 0.08 0.2651 ± 0.01 1.00 0.76 0.95
PP 1.1315 ± 0.2 1.4868 ± 0.21 0.3553 ± 0.04 0.92 0.29 0.37
PES 0.1935 ± 0.03 0.3059 ± 0.04 0.1127 ± 0.03 1.38 0.20 0.66
PA 0.2965 ± 0.02 0.4135 ± 0.03 0.1170 ± 0.03 1.15 0.15 0.82

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Figure 4. Time-dependent adsorption of 1 mg·L−1 Pb from seawater to virgin (V) and biofilm-covered (B) PE-(a), PP-(b), PES-(c), and PA-(d)
MFs at 22 ° C (MFs = 10 g·L−1). Error bars represent the standard error (0.0001−0.04) of the mean of three determinations, and dotted lines are
fits to the data based on the PFO and PSO models shown in Supporting Information Table S2 and constants provided in Supporting Information
Table S3.

Figure 5. Fitting of the isotherm data of Pb adsorption: concentration-dependent adsorption of 1−10 mg·L−1 Pb from seawater to virgin (V) and
weathered (B) PE (a), PP (b), PES (c), and PA (d) MFs at room temperature (MF dose = 10 g·L−1, pH = 7.8). Error bars represent the standard
error (0.001−0.004) about the mean of three determinations, and dotted lines are fits to the data based on the Langmuir and Freundlich isotherms
described previously in Table S2 whose constants are provided in Table S4.

(2.57 ± 6 × 10−3 μg·g−1) and PA-BMF (3.33 ± 3 × 10−3 μg· could be due to the presence of polarized N−H bonds in the
g−1) samples. In general, the increment in KD due to biofilms polymer chain of PA that can facilitate PFOS partitioning
followed the order PA<PES<PE<PP (values in Table 2). because of hydrophobic interactions and hydrogen bonding
These results are similar to other studies available in the mechanisms.72
literature (Supporting Information Table S10) that have The adsorption isotherm of PFOS (Figure 7) on VMF and
reported approximately 78, 45, and 100% adsorption on PE, BMF followed both the Freundlich model and linear model, as
PP, and PA MPs.11 The highest adsorption of PFOS on PA indicated by the correlation coefficient and mean squared error
was also reported in a recent study in which the adsorption of (MSE) values provided in Supporting Information Table S8.
multiple micropollutants on nine different environmentally The increase in PFOS adsorption in biofilm-covered samples
aged MPs was compared.11 The high adsorption of PFOS was significantly (p < 0.05) high compared to that in their
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virgin counterparts. Biofilm-covered samples adsorbed 13.54 ±

0.1, 16.24 ± 0.43, 16.36 ± 0.07, and 17.03 ± 0.12 μg·g−1 in
PE-BMF, PP-BMF, PES-BMF, and PA-BMF from 100 μg·L−1
spiking solution which was 35.6 ± 0.4, 64.6 ± 0.8, 25.4 ± 0.2,
and 37.27 ± 0.4% higher than their virgin counterparts. Values
for the equilibrium parameter RL, calculated from the
Langmuir eq (Supporting Information Table S9), were in
the range of 0−1, indicating that the adsorption process of
PFOS on all MF was favorable.
3.4. Desorption of Pb and PFOS from Plastic MFs.
Desorption of Pb, as shown in Figure 8A, reached equilibrium

Figure 6. Time-dependent adsorption of 20 μg·L−1 PFOS from

seawater to virgin (V) and biofilm-covered (B) PE (A), PP (B), PES
(C), and PA (D) MFs at room temperature (MFs = 5 g·L−1). Error
bars represent the standard error (0.004−0.01) about the mean of Figure 8. (A) Desorption of Pb at equilibrium concentrations in
three determinations, and dotted lines are fits to the data based on the seawater at pH 7.8, 22 °C from MF spiked with 1 mg·L−1 of Pb and
PFO model, as described previously in Table S2, whose constants are (B) Desorption of PFOS at equilibrium concentrations in seawater at
provided in Table S7. pH 7.8, 22 °C from MF spiked with 20 μg·L−1 of PFOS.

Table 2. Partition/Distribution Coefficient for PFOS for

after 8−10 h in the VMF samples and 10−14 h in the BMF
PE, PP, PES, and PA MFs after 30 Days in Seawater
samples (Supporting Information Table S11). The desorption
samples KD biofilm-covered KD of Pb from VMF was higher and quicker than that from BMF
V-PE 86.2 B-PE 254.7 but not statistically significant. These results suggest that
V-PP 76.0 B-PP 208.9 biofilms could potentially reduce the desorption of contami-
V-PES 272.9 B-PES 587.0 nants from the surface of MF by the creation of metal
V-PA 426.2 B-PA 995.0 complexes.73−75 PFOS desorption, as indicated in Figure 8B,
reached equilibrium after 48 h in VMF and 60 h in the BMF
samples (Supporting Information Table S12). Similarly, the
desorption of PFOS from VMF was higher than that from
BMF and was statistically significant in all sample types.
Studies have indicated that PFOS partition to the phospholipid
and EPS in biofilms76 would have allowed their retention in
the biomass and influence desorption.
3.5. Biofilm-Enhanced Adsorption of Contaminants
and Environmental Implications. The distribution and
adsorption−desorption of contaminants to and from MPs is an
essential factor that affects the contaminant’s residual
concentration, migration, transformation, bioavailability, and
toxicity in the environment. This study validated the
hypothesis and demonstrated that the growth of biofilm varied
by the polymer type and significantly influenced the adsorption
of Pb and PFOS on MFs to varying degrees depending on the
polymer type. The good fit of the experimental results to the
kinetic models sheds light on the adsorption mechanisms.
Some studies on other metals such as Cu, Cd, and so forth
Figure 7. Fitting of the isotherm data of PFOS adsorption: have indicated that the functional groups in microbial biofilms
concentration-dependent adsorption of 5−100 μg·L−1 PFOS from play a crucial role in metal complexation.77−79 Studies have
seawater to virgin (V) and weathered (B) PE (a), PP (b), PES (c),
also shown that biofilms occupy high-energy sorption sites and
and PA (d) MFs at room temperature (MFs = 5 g·L−1). Error bars
represent the standard error (0.007−0.43) about the mean of three exhibit significant effects on the transport and adsorption of
determinations, and dotted lines are fits to the data based on organic pollutants via cumulative sorption and cosorption in
Langmuir and Freundlich isotherms described previously in Table S2, soil, nanoparticles, and PE.80−82
whose constants are provided in Table S8. The current literature along with the results from this study
strongly indicates that biofilms play a crucial role in enhancing
the accumulation of contaminants on MPs that could exhibit a
number of serious environmental implications. The formation
8883 https://doi.org/10.1021/acs.est.1c02012
Environ. Sci. Technol. 2021, 55, 8877−8887
Environmental Science & Technology pubs.acs.org/est Article

of biofilms on MPs may generate a chemosensory response models and isotherm, and comparison of results with
because of which MPs become more bioavailable and palatable studies in the literature and details of desorption (PDF).
for ingestion by organisms at both lower83 and higher trophic

■
levels.84 Furthermore, the enhanced accumulation of con-
taminants on MPs due to biofilms may lead to a higher AUTHOR INFORMATION
bioaccumulation of MP-associated PFOS,85 Pb,86 and other
toxic contaminants.87 This, in turn, may lead to the Corresponding Author
biomagnification of toxic contaminants in the aquatic food Thava Palanisami − Global Innovative Centre for Advanced
web 88−90 and have implications on human health. 91 Nanomaterials, College of Engineering, Science and
Furthermore, the attachment and detachment of biofilms Environment, The University of Newcastle, Callaghan, New
from MPs along with sorbed contaminants can also present South Wales 2308, Australia; orcid.org/0000-0003-
challenges in assessing the accurate risk assessment. 2344-1493; Email: [email protected]
Ion exchange has been discussed in the literature as the
major mechanism of metal ion adsorption in biofilms.92 For Authors
instance, Cu+2 adsorption in biofilms was shown to result in Geetika Bhagwat − Global Innovative Centre for Advanced
the binding of Cu+2 with the hydroxyl groups and amide Nanomaterials, College of Engineering, Science and
groups present in the extracellular polymeric substances found Environment, The University of Newcastle, Callaghan, New
in the biofilms.93 This suggests that metal ions can be used as a South Wales 2308, Australia
nutrient by the organisms in the biofilms to maintain a Thi Kim Anh Tran − Global Innovative Centre for Advanced
sustainable, nutrient-rich environment within the biofilms Nanomaterials, College of Engineering, Science and
through both ion adsorption and desorption. However, the Environment, The University of Newcastle, Callaghan, New
adsorption and complexation reactions involving toxic metals South Wales 2308, Australia
such as Pb are known to be governed by the tolerance Dane Lamb − Global Innovative Centre for Advanced
potential of microorganisms.94 For instance, a recent study that Nanomaterials, College of Engineering, Science and
explored the composition and function of microbes in Environment, The University of Newcastle, Callaghan, New
environmental biofilms on four types of MPs indicated the South Wales 2308, Australia; orcid.org/0000-0003-
enrichment of microbial genera involved in xenobiotic 2303-5460
compound degradation and heavy-metal-resistance gene Kala Senathirajah − Global Innovative Centre for Advanced
clusters on all plastic types.16 This indicates that the Nanomaterials, College of Engineering, Science and
composition of biofilms can significantly influence the Environment, The University of Newcastle, Callaghan, New
transport and fate of metals in the aquatic environment. South Wales 2308, Australia
Another study showed a high accumulation of metals and Ian Grainge − School of Environmental and Life Sciences,
PFAS on 10-year aged plastics41 and showed the presence of College of Engineering, Science and Environment, The
bacterial genus Pseudoalteromonas, Psychrobacter, and Oceano- University of Newcastle, Callaghan, New South Wales 2308,
sphaera known to prefer a surface-associated lifestyle and Australia
potential for organic compounds and polymer degradation. Wayne O’Connor − NSW Department of Primary Industries,
This study was conducted at a site very close to the Port Stephens Fisheries Institute, Taylors Beach, New South
aquaculture ponds used for aging the ropes used in the Wales 2316, Australia
present study, suggesting that the presence of such genera may Albert Juhasz − Future Industries Institute, University of South
influence the adsorption and subsequent metabolism of such Australia, Adelaide, South Australia 5095, Australia
compounds under natural conditions. The study further Complete contact information is available at:
highlighted the lack of data on the processes of desorption, https://pubs.acs.org/10.1021/acs.est.1c02012
readsorption, detachment, and dissolution of plastic-associated
biofilms and inorganic matter and its role as a source and/or Author Contributions
sink for environmental contaminants. Therefore, studies that G.B.: Project administration, writing original draft, conceptu-
show the marrying of the sorption kinetics and modeling of
alization, and methodology; K.A.T.: Project administration,
MP particle hydrodynamic distribution, as well as studies that
validation, review, and editing; K.S. and I.G.: Review and
investigate the interactions of biomolecules that constitute
biofilms with environmental contaminants will provide editing; W.O.C.: Resources, review, and editing; D.L.:
important information on the impact of biofilms on the Resources, formal analysis; A.J.: Formal analysis; I.G.: Formal
behavior of MPs in the aquatic environment. analysis, T.P.: Supervision, review and editing, project support,

■
and funding acquisition.
ASSOCIATED CONTENT Notes
*
sı Supporting Information The authors declare no competing financial interest.
The Supporting Information is available free of charge at
https://pubs.acs.org/doi/10.1021/acs.est.1c02012.
Details of methods for FTIR, SEM, and EDS analysis,
■ ACKNOWLEDGMENTS
The authors acknowledge the support provided by the
biofilm quantification, microplastic characterization, Commonwealth of Australia and the University of Newcastle,
instrument analysis and validation for ICP-MS and Australia, through the Australian Government Research
LC−MS/MS, physicochemical characterization of water, Training Program (RTP) Scholarship. The authors wish to
details of adsorption kinetic and isotherm models, QA/ thank Dr. Kavitha Ramadass and Rohan Bahadur for their
QC and statistical methods, parameter values for kinetic assistance with PFOS and SEM analyses.
8884 https://doi.org/10.1021/acs.est.1c02012
Environ. Sci. Technol. 2021, 55, 8877−8887
Environmental Science & Technology

■
pubs.acs.org/est Article

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