Biologically mediated abiotic degradation (BMAD) of bisphenol A by manganese-oxidizing bacteria

Article abstract of DOI:10.1016/j.jhazmat.2021.125987

Bisphenol A (BPA), a chemical of environmental concern, is recalcitrant under anoxic conditions, but is susceptible to oxidative degradation by manganese(IV)-oxide (MnO₂). Microbial Mn(II)-oxidation generates MnO_2-bio; however, BPA degradation in cultures of Mn(II)-oxidizing bacteria has not been explored. We assessed MnO_2-bio-mediated BPA degradation using three Mn(II)-oxidizing bacteria, Roseobacter sp. AzwK-3b, Erythrobacter sp. SD-21, and Pseudomonas putida GB-1. In cultures of all three strains, enhanced BPA degradation was evident in the presence of Mn(II) compared to replicate incubations without Mn(II), suggesting MnO_2-bio mediated BPA degradation. Increased Mn(II) concentrations up to 100 μM resulted in more MnO_2-bio formation but the highest BPA degradation rates were observed with 10 μM Mn(II). Compared to abiotic BPA degradation with 10 μM synthetic MnO₂, live cultures of strain GB-1 amended with 10 μM Mn(II) consumed 9-fold more BPA at about 5-fold higher rates. Growth of strain AzwK-3b was sensitive to BPA and the organism showed increased tolerance against BPA in the presence of Mn(II), suggesting MnO_2-bio alleviated the inhibition by mediating BPA degradation. The findings demonstrate that Mn(II)-oxidizing bacteria contribute to BPA degradation but organism-specific differences exist, and for biologically-mediated-abiotic-degradation (BMAD), Mn-flux, rather than the absolute amount of MnO_2-bio, is the key determinant for oxidation activity.

Full text of DOI:10.1016/j.jhazmat.2021.125987

Journal of Hazardous Materials 417 (2021) 125987
Contents lists available at ScienceDirect
Journal of Hazardous Materials
journal homepage: www.elsevier.com/locate/jhazmat
Biologically mediated abiotic degradation (BMAD) of bisphenol A by
manganese-oxidizing bacteria
a
,
1
b
,
c
a
b,c,d,e,f
Nusrat Shobnam , Yanchen Sun , Maheen Mahmood , Frank E. L o¨ ffler
Jeongdae Im
,
a,*
a
Department of Civil Engineering, Kansas State University, Manhattan, KS 66506, USA
Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN 37996, USA
Center for Environmental Biotechnology, University of Tennessee, Knoxville, TN 37996, USA
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA
b
c
d
e
f
Department of Microbiology, University of Tennessee, Knoxville, TN 37996, USA
Department of Biosystems Engineering and Soil Science, University of Tennessee, Knoxville, TN 37996, USA
A R T I C L E I N F O
A B S T R A C T
Editor: Dr. R. Debora
Bisphenol A (BPA), a chemical of environmental concern, is recalcitrant under anoxic conditions, but is sus-
ceptible to oxidative degradation by manganese(IV)-oxide (MnO ). Microbial Mn(II)-oxidation generates MnO2-
2
Keywords:
bio; however, BPA degradation in cultures of Mn(II)-oxidizing bacteria has not been explored. We assessed MnO2-
bio-mediated BPA degradation using three Mn(II)-oxidizing bacteria, Roseobacter sp. AzwK-3b, Erythrobacter sp.
SD-21, and Pseudomonas putida GB-1. In cultures of all three strains, enhanced BPA degradation was evident in
the presence of Mn(II) compared to replicate incubations without Mn(II), suggesting MnO2-bio mediated BPA
degradation. Increased Mn(II) concentrations up to 100 µM resulted in more MnO2-bio formation but the highest
Endocrine disrupting chemicals
Reactive mineral phases
Manganese cycle
Coupled biotic-abiotic processes
BPA degradation rates were observed with 10 µM Mn(II). Compared to abiotic BPA degradation with 10
μ
M
synthetic MnO , live cultures of strain GB-1 amended with 10 M Mn(II) consumed 9-fold more BPA at about 5-
2
μ
fold higher rates. Growth of strain AzwK-3b was sensitive to BPA and the organism showed increased tolerance
against BPA in the presence of Mn(II), suggesting MnO2-bio alleviated the inhibition by mediating BPA degra-
dation. The findings demonstrate that Mn(II)-oxidizing bacteria contribute to BPA degradation but organism-
specific differences exist, and for biologically-mediated-abiotic-degradation (BMAD), Mn-flux, rather than the
absolute amount of MnO2-bio, is the key determinant for oxidation activity.
1
. Introduction
bacteria, fungi, algae, and plants have been demonstrated to degrade
BPA under oxic conditions (Staples et al., 1998; Im and L o¨ ffler, 2016;
Bisphenol A (BPA) is a high production volume chemical for the
manufacture of polycarbonate plastic and epoxy resins (Staples et al.,
998; Crain et al., 2007; Rochester, 2013). The global demand of BPA
Zhang et al., 2013). Under anoxic conditions, several studies concluded
that BPA is recalcitrant (Kang and Kondo, 2002, 2005; Voordeckers
et al., 2002; Im et al., 2014a), until recent efforts demonstrated that
chemically synthesized manganese dioxide (MnO2-syn) mediated BPA
transformation and mineralization without oxygen requirement (Lin
et al., 2009, 2013; Im et al., 2015; Balgooyen et al., 2017; Huang et al.,
2018; Saroyan et al., 2019). GC/MS analysis detected a number of
transformation products (Lin et al., 2009), and hydroxycumyl alcohol
(HCA) was identified as a major intermediate (Im et al., 2015, 2014b;
Balgooyen et al., 2017; Wang et al., 2018).
1
exceeded 7.7 million tons in 2015 and is predicted to grow (Industry
Experts, 2017). Low concentrations of BPA detected in sediment and
surface waters (Bolz et al., 2001; Heemken et al., 2001; Kleck
̌
a et al.,
2
009) and possible risks of human exposure (Hengstler et al., 2011;
Sekizawa, 2008) triggered substantial efforts exploring the environ-
mental fate of BPA (Staples et al., 1998; Im and L o¨ ffler, 2016). With a
K
OW of 3.42, BPA is susceptible to adsorption by suspended solids and
solid matrices (e.g., sediments) (Staples et al., 1998). Diverse taxa of
2
MnO is a naturally occurring, strong oxidant, abundant in anoxic
*
Correspondence to: Kansas State University, Department of Civil Engineering, 1701C Platt ST, Manhattan, KS 66506, USA.
E-mail address: jeongdaei@ksu.edu (J. Im).
1
Present address: Govind Development, LLC, 9510 Leopard St., Corpus Christi, TX 78410, USA.
https://doi.org/10.1016/j.jhazmat.2021.125987
Received 29 January 2021; Received in revised form 28 April 2021; Accepted 28 April 2021
Available online 3 May 2021
0
304-3894/© 2021 Elsevier B.V. All rights reserved.

N. Shobnam et al.
Journal of Hazardous Materials 417 (2021) 125987
soils as well as marine and freshwater sediments (Vandieken et al., 2012;
Sigg et al., 1987). Therefore, its efficacy to oxidize organic (e.g., anti-
bacterial agents, pesticides, endocrine disruptors, and heterocyclic
compounds) (Remucal and Ginder-Vogel, 2014; Sochacki et al., 2018;
metal solution containing: 0.04
μ
M copper sulfate, 0.15 M zinc sulfate,
μ
0.08 M cobalt chloride, 0.06 M sodium molybdate and 10 mM HEPES
μ
μ
buffer pH 7.5) (Banh et al., 2013). Culture vessels (250-mL Erlenmeyer
flasks) containing 100 mL of medium were capped with aluminum foil
-
◦
Zhang et al., 2017) and inorganic (e.g., HS , heavy metals) (Miyata et al.,
and incubated at 30 C and on a rotary shaker (120 rpm) in the dark.
2
007; Hennebel et al., 2009; Villalobos et al., 2005) contaminants has
been widely investigated. The formation of MnO mineral phases is not
2
fully understood, but it is believed to be mainly attributed to microbial
activities (Tebo et al., 2004; Learman et al., 2011). Biologically pro-
duced reactive mineral phases have attracted attention for their roles in
the degradation of priority pollutants in subsurface environments, and
biologically-mediated abiotic degradation (BMAD) has drawn attention
as a sustainable remediation approach (Im et al., 2014b; He et al., 2015;
Nied ´z wiecka and Finneran, 2015; Kwon et al., 2011; Perreault et al.,
2.3. MnO2-bio formation and BPA degradation
Typical levels of Mn(II) in freshwater range from 0.02 to 4
Mn(II) concentrations up to 200 M have been reported (USEPA, 2004).
To determine the effect of Mn(II) concentrations on MnO2 formation,
μ
M and
μ
-bio
cultures of strain AzwK-3b, strain SD-21 and strain GB-1 received 0, 10,
100, and 500 M Mn(II) in the absence of BPA. Replicate experiments
tested the effects of Mn(II) concentrations on BPA degradation in strain
SD-21 and strain GB-1 cultures that received 18 M BPA. Strain AzwK-3b
μ
2
012). Many microorganisms, including bacteria and fungi, are known
to catalyze Mn(II) oxidation leading to the formation of MnO in natural
2
μ
and engineered environments (Tebo et al., 2004). The few studies that
examined the role of Mn(II)-oxidizing bacteria (MOB) controlling the
environmental fate of contaminants used either purified, cell-free
MnO2-bio (Kim et al., 2012; Forrez et al., 2010, 2011; Tran et al.,
cultures received a lower BPA concentration as we determined inhibi-
tory effects on growth when at concentrations exceeding 9 µM. Potential
inhibition of BPA on the growth of each bacterial species was assessed in
K-ASW-medium with 0, 9, 18 and 44
The effect of Mn(II) on BPA inhibition observed in strain AzwK-3b cul-
tures was examined with 18 M BPA in the absence or presence of 100
M Mn(II). BPA was added before sterilization of the culture medium
μM BPA in the absence of Mn(II).
2
018) or mixed cultures (Sochacki et al., 2018; Forrez et al., 2009;
Zhang et al., 2015). A recent study demonstrated the degradation of
cylindrospermopsin, an alkaloid cyanotoxin, using Mn(II)-oxidizing
bacterial isolates in the presence of exogenous Mn(II) (Martínez-Ruiz
et al., 2020b, 2020a). Although BPA degradation by MnO2-syn has been
extensively studied (Im and L o¨ ffler, 2016; Remucal and Ginder-Vogel,
μ
μ
and Mn(II) was added from sterile 100 mM MnCl stock solutions. Un-
2
inoculated (sterile) medium incubations served as negative controls. All
experiments were performed in triplicate. Pseudo-first order kinetics
were assumed based on the linearity observed during the initial stage of
incubation (Im et al., 2015; Forrez et al., 2010; Tran et al., 2018; Liao
et al., 2016). The pseudo-first-order rate constants (k) were obtained by
plotting the natural log of BPA concentrations as a function of time (i.e.,
2
014), the potential impact of microbial Mn(II) oxidation (i.e., BMAD)
on BPA is uncertain.
To assess the validity of the BMAD principle, we assessed BPA
degradation in cultures of the three extensively studied MOB including
Roseobacter sp. strain AzwK-3b, Erythrobacter sp. strain SD-21, and
Pseudomonas putida strain GB-1. These MOB species were selected on the
basis of distinct Mn(II) oxidation mechanisms. Strain AzwK-3b oxidizes
Mn(II) indirectly through the enzymatic formation of extracellular
reactive oxygen species (ROS), specifically superoxide radicals (Lear-
-
1
k = -Δ(ln C ) Δt ) using three early time points, where linear relation-
t
ships were observed. The standard deviation of the slope was deter-
mined using the LINEST function in Excel 2016 (Microsoft Corp.,
Redmond, WA). To verify that adsorption was negligible even at the
highest observed OD600 value for each strain, a validated methanol
extraction procedure (Im et al., 2016) was employed, which confirmed
that sorptive losses of BPA were marginal. Briefly, each strain grown to
stationary phase in the absence of BPA and Mn(II) was centrifuged for
man et al., 2011). Strain SD-21 utilizes a Ca2 -binding heme peroxidase
+
(
Anderson et al., 2009), and strain GB-1 employs multicopper oxidases
and peroxidase cyclooxygenases (also referred to as animal heme per-
oxidases) to oxidize Mn(II) (Geszvain et al., 2016). The findings imply
that Mn flux, rather than the absolute amount of MnO2-bio, is a key
determinant for BMAD activity, and highlight that oxic-anoxic transition
10 min at 10,000g and resuspended in fresh medium containing 18 M
μ
BPA. After 1-min incubation, triplicate 0.75-mL aliquots of cell sus-
pension were centrifuged, and the supernatant was collected for
aqueous phase BPA analysis. The total BPA concentrations were ob-
tained by a methanol extraction procedure (Im et al., 2016). Therefore,
for quantification of BPA and HCA in live cultures, 1-mL aliquots of
culture suspensions were centrifuged for 10 min at 10,000g without
methanol extraction, and the supernatant was subjected to HPLC
analysis.
zones with active Mn cycling are potential hotspots for MnO
BPA degradation.
2
-mediated
2
. Materials and methods
.1. Chemicals and preparation of MnO2-syn
BPA (> 99% purity), MnCl O (> 98% purity), leucoberbelin
× 4H
2
2
2
blue (LBB, 65% dye content), and L-ascorbic acid were purchased from
Sigma-Aldrich (St. Louis, MO). Metyrapone [2-methyl-1,2-di-(3-
pyridyl)ꢀ 1-propanone] was purchased from Cayman Chemical Com-
pany (Ann Arbor, MI). MnO2-syn was prepared according to established
procedures (see Supplementary Material) (Kostka and Nealson, 1998),
and HCA (> 95% purity confirmed by NMR) was synthesized as pre-
2.4. Abiotic BPA degradation by MnO2-syn
To compare the BPA degradation efficiency of MnO2-syn and MnO2-
bio, abiotic BPA degradation kinetics were determined under sterile
conditions using 10 M MnO2-syn (nominal concentration) as previously
μ
described (Im et al., 2015), and the degradation rates and extents were
compared with those from biological incubation of strain GB-1 amended
viously described (Im et al., 2015). TraceMetal grade HNO
3
(67–70%,
wt/wt) was purchased from Fischer Scientific (Hampton, NH).
with 10
conducted in 160-mL glass serum bottles with a total volume of 100 mL
containing 18 M BPA in 5 mM potassium phosphate buffer at pH 7. BPA
degradation was initiated by adding MnO2-syn from a 0.4 M sterile stock
suspension to achieve a final nominal concentration of 10 M. Aliquots
(0.5 mL) of the reaction mixture were collected periodically and trans-
μM Mn(II). Briefly, experiments performed in triplicate were
2
.2. Strains and culturing conditions
μ
Strain AzwK-3b and strain SD-21 were maintained in an organic-rich
μ
K-medium (2 g L-1 peptone, 0.5 g L yeast extract, 20 mM HEPES buffer,
-1
pH 7.5) prepared with 75% (vol/vol) artificial seawater (K-ASW)
ferred to 2-mL glass HPLC vials containing 20
μ
L of L-ascorbic acid so-
-
1
ꢀ 1
(
Learman et al., 2011). Strain GB-1 was grown in Lept medium (0.5 g L
lution (50 mg mL ) and immediately vortexed for 5 s. L-ascorbic acid
quenches the reaction by converting any remaining MnO2-syn to soluble
Mn(II), which liberates any sorbed BPA (Im et al., 2015).
-
1
yeast extract, 0.5 g L casamino acids, 5 mM glucose, 0.48 mM calcium
chloride, 0.83 mM magnesium sulfate, 3.7 M iron (III) chloride, trace
μ
2

N. Shobnam et al.
Journal of Hazardous Materials 417 (2021) 125987
2
.5. BPA degradation in the absence of Mn(II)
Cytochrome P450 monooxygenase systems can contribute to BPA
degradation and demonstrated in Sphingomonas sp. strain AO1 (Sasaki
et al., 2005b). Both strain AzwK-3b and strain SD-21 possess genes
encoding putative cytochrome P450s enzyme systems. To examine if
cytochrome P450 contributes to cometabolic BPA degradation, metyr-
apone, a known cytochrome P450 inhibitor, was used. Strain AzwK-3b
and strain SD-21 were incubated in K-ASW-medium in the presence
and absence of 0.5 mM metyrapone (Kolvenbach et al., 2007). To
confirm that traces of Mn(II) in yeast extract did not impact BPA
degradation by strain AzwK-3b and strain SD-21 in the absence of
exogenous Mn(II), additional experiments were performed using a Mn
Fig. 1. Effects of Mn(II) concentrations on MnO2-bio formation in the absence of
BPA. Error bars represent the standard deviations of triplicate samples of
triplicate cultures.
(
II)-free defined mineral salt medium. Strain AzwK-3b and strain
SD-21 were incubated in a J-Acetate medium consisting of 10 mM so-
-
1
dium acetate, 10 mL L Wolfe’s vitamin supplement (Wolin et al.,
1
7
7
2
963), 1.5 mM NH
4
Cl, 2 mM KHCO
3
, 73
μ
M KH
2
PO
4
, 3.6
μ
M FeSO
4
×
concentrations higher than 100
tory effects of Mn(II) on MnO -mediated contaminant degradation have
been attributed to the passivation of the MnO surface (Lin et al., 2009,
013), but a detailed mechanistic understanding of the inhibition of Mn
II) oxidation by excess Mn(II) has not been attained.
μM (Sabirova et al., 2008). The inhibi-
H
2
O complexed with 78
μM nitrilotriacetic acid, 20 mM HEPES (pH
.6), and prepared with 50% (vol/vol) artificial seawater (Estes et al.,
017).
2
2
2
(
2
.6. Analytical procedures
An Agilent 1100 Series HPLC system equipped with a fluorescence
3
.2. Enhanced BPA degradation in the presence of Mn(II)
detector (FLD) was used for the detection and quantification of BPA and
HCA. A reversed-phase Agilent Eclipse XDB C18 column (4.6 mm × 150
To evaluate the effect of Mn(II) on BPA degradation, each culture
mm, 5 µm) was used for isocratic separation with an acetonitrile-water
50:50, vol/vol) eluent at a flow rate of 1 mL min- (Im et al., 2015).
1
was first incubated with BPA in the absence of Mn(II). BPA degradation
was observed in cultures of strain AzwK-3b and strain SD-21, but not in
cultures of strain GB-1 (Fig. 2). For all three MOB cultures, enhanced
BPA degradation was evident in the presence of Mn(II) compared to
replicate incubations without Mn(II) (Fig. 3a–c and Fig. S2a–f), sug-
gesting that MOB produced MnO2-bio, which subsequently mediated
abiotic BPA degradation (i.e., the BMAD process). Interestingly, the
amount of MnO2-bio produced in the different cultures did not correlate
with the observed BPA degradation rates. The highest amounts of MnO2-
(
MnO
Altmann, 1973) relative to a standard curve prepared with KMnO
standard curve preparation, 30 L of KMnO dilutions spanning a con-
centration range from 7 to 100 µM were aliquoted into empty wells of a
6-well microtiter plate followed by the addition of 270 L LBB solution
40 mg LBB in 100 mL 45 mM acetic acid). For MnO2-bio quantification
in live cultures, 50 L samples were collected in 2-mL microcentrifuge
tubes and mixed with 450 L LBB solution. Samples of MnO2-syn were
2
was quantified using a colorimetric LBB assay (Krumbein and
4
. For
μ
4
9
μ
(
μ
μ
bio were observed in incubations with 100 M Mn(II) for all three spe-
μ
diluted and mixed with LBB solution at a ratio of 1:10. All samples were
incubated at room temperature for 15 min in the dark, centrifuged for 1
cies, but the Mn(II) concentrations that resulted in the highest observed
BPA degradation rates were lower. For strain AzwK-3b and strain GB-1,
min at 10,000g to pellet solids, and 300 L of the supernatant was
μ
-
1
the highest BPA degradation rates of 0.44 ± 0.09 and 0.23 ± 0.02 day ,
respectively, were observed with 10 M Mn(II), even though about 10-
times lower amounts of MnO2-bio were generated compared to in-
cubations with 100 M Mn(II) (Fig. 3a, c; Fig. S2a, b, e, f). Strain SD-21
consumed BPA at rates of 1.33 ± 0.52 day with 100
(Fig. 3b, Fig. S2c, d), and a similar rate of 0.92 ± 0.42 day was
measured in cultures with 10 M Mn (II) (P > 0.1) although 10-times
transferred to a flat bottom 96-well microtiter plate. Absorbance was
measured at 618 nm using an Epoch 2 microplate spectrophotometer
μ
(
BioTek Instruments, Inc., Winooski, VT). Growth of the strains was
μ
monitored by measuring absorbance of live cultures at 600 nm using the
same instrument. To dissolve MnO2-bio and prevent any interferences
-
1
μ
M Mn(II)
-
1
ꢀ
1
with the growth measurements, L-ascorbic acid (12 L of a 50 mg mL
μ
μ
stock solution) was added to individual wells. The total Mn(II) con-
centrations were measured using Inductively Coupled Plasma Mass
Spectrometry (ICP-MS). The samples (5 mL) were filtered through a
0
.45-
μ
m nitrocellulose membrane filter (Millipore Corp., Bedford, MA)
and acidified with 30
μ
L HNO
3
(67–70%, wt/wt). A Students’ t-test was
performed to test the significance of any difference between the means
and a p-value < 0.05 value was considered to be statistically significant.
3
. Results and discussion
3
.1. Effect of Mn(II) on MnO2-bio formation
In cultures of all three bacterial species tested, the maximum nomi-
nal MnO2-bio concentrations increased with increasing Mn(II) concen-
trations up to 100 M. At the highest Mn(II) concentration tested (500
M), lower MnO2-bio concentrations were observed in cultures of strain
SD-21 and strain GB-1 or did not result in a further increase of MnO2-bio
strain AzwK-3b; P > 0.1) (Fig. 1 and Fig. S1a–c). The observation that
elevated Mn(II) concentrations negatively affect MnO formation is not
μ
μ
Fig. 2. Growth and co-metabolic degradation of BPA by strain AzwK-3b, strain
SD-21, and strain GB-1 in the absence of Mn(II). The solid lines represent C/C
(
0
2
BPA concentrations, and the dashed lines show the cell growth based on OD600
nm absorbance measurements. Error bars represent the standard deviations of
triplicate samples. Error bars smaller than the symbol size are not depicted.
unprecedented and has been reported for Leptothrix discophora and
Pseudomonas putida strains MB1, MB6, and MB29 at Mn(II)
3

N. Shobnam et al.
Journal of Hazardous Materials 417 (2021) 125987
Fig. 3. BPA degradation and MnO
2
formation in cultures of Mn(II)-oxidizing bacteria amended with different Mn(II) concentrations. The columns show maximum
nominal MnO2-bio concentrations, and the diamonds show BPA degradation rates. Panels (a), (b) and (c) show MnO
2
formation and BPA degradation rates in cultures
of strain AzwK-3b, strain SD-21, and strain GB-1, respectively. Error bars represent the standard deviations of triplicate cultures.
more MnO2-bio was formed in vessels with 100 M Mn(II) (Fig. S2d).
μ
Similar observations were made with Leptothrix discophora strain SS-1
and Pseudomonas putida strains MB1, MB6, and MB29; i.e., increasing
amounts of MnO2-bio were generated but the rates of 17 -ethinylestra-
α
diol degradation did not increase in the presence of elevated concen-
trations of Mn(II) (Sabirova et al., 2008). Several studies also
demonstrated that the removal of organic contaminants was signifi-
cantly lower or came to a complete halt when microbial activity was
precluded by heat treatment or sodium azide additions (Sochacki et al.,
2
018; Tran et al., 2018; Meerburg et al., 2012). These findings empha-
size the relevance of BMAD for contaminant turnover, and suggest that
Mn flux, rather than the absolute amount of MnO2-bio, is the relevant
metric and a potentially useful measure to gauge the MnO2-bio-mediated
contaminant transformation activity. Unfortunately, robust tools to
determine in situ Mn(II) fluxes in environmental systems are not
available.
Fig. 4. Degradation of BPA in abiotic incubations with 10
versus biotic incubations with 10
M of Mn(II). No more than 2.1 ± 0.3 µM BPA
was degraded in sterile abiotic incubations with 10 M of MnO2-syn over a 17-
day incubation period. In incubations with 10 M Mn(II) inoculated with
Pseudomonas putida strain GB-1, the initial amount of 18 BPA was
μ
M of MnO2-syn
μ
μ
In sterile abiotic experiments with MnO2-syn, 10 µM MnO2-syn
-
1
μ
degraded 2.1 ± 0.3 µM BPA at a rate of 0.06 ± 0.0.03 day . In live
μ
M
cultures of strain GB-1 amended with 10 M Mn(II), about 5-fold higher
μ
completely consumed. Error bars represent the standard deviations of triplicate
samples of triplicate cultures. Error bars smaller than the symbol size are
not depicted.
-
1
BPA degradation rate of 0.30 ± 0.07 day was observed and 9-fold
more BPA (18.5 ± 0.4 µM) was consumed (Fig. 4). These findings sug-
gest that Mn cycling and regeneration of MnO2-bio occurred in the live
cultures, resulting in more effective BPA degradation. Microbial Mn(II)
oxidation coupled with Mn(IV)-mediated BPA degradation constitutes
an efficient cycle, and a small amount of Mn can turnover a substantial
amount of BPA (Fig. 5). A recent study demonstrated light-driven Mn(II)
2
oxidation in microbial biofilms in the absence of O (Daye et al., 2019),
suggesting that BMAD processes that act on BPA are not limited to
oxic-anoxic transition zones but can also be expected in the photic zones
of anoxic water bodies.
Strain AzwK-3b cultures that received 100
produced similar amounts of MnO2-bio (80.5 ± 0.4
2.4 ± 0.3 M, respectively), but BPA degradation rates decreased from
μ
M or 500
μ
M Mn(II)
μ
M versus
Fig. 5. Schematic illustration of biologically mediated abiotic degradation
8
μ
of BPA.
4

N. Shobnam et al.
Journal of Hazardous Materials 417 (2021) 125987
-
1
0
.39 ± 0.10 to 0.25 ± 0.06 day (Fig. 3a). A plausible explanation is
sorption of excess Mn(II) to solid phase MnO , which impacted the
reactivity of MnO2-bio. MnO has been reported to have high adsorption
MnO2-syn-mediated BPA degradation (i.e., 50–64%) (Fig. 6), suggesting
that MnO2-bio and MnO2-syn are functionally equivalent and/or HCA was
not readily consumed by both strains. For strain SD-21, a much lower
BPA-to-HCA conversion efficiency of 20% was determined (Fig. 6),
suggesting that HCA was (co-)metabolically degraded as it was formed,
which is plausible given the high BPA degradation rate observed in this
strain in the absence of Mn(II) (Fig. 2).
2
2
capacities for metal ions, and suppression of BPA degradation by MnO2-
syn has been reported in the presence of Mn(II) (Lin et al., 2009, 2013).
3
.3. Inhibitory effect of BPA on strain AzwK-3b and relief of inhibition by
MnO2-bio
3
.5. Effect of trace Mn in peptone and yeast extract on BPA degradation
In the absence of Mn(II), BPA concentrations of up to 9 µM had no
effect on growth of strain AzwK-3b and similar growth rates ranging
in the absence of exogenous Mn(II)
-
1
-1
between 2.77 ± 0.32 day
P > 0.1). At BPA concentrations of 18 µM and higher, inhibition was
observed (P < 0.05) and the first order growth rate declined to
and 3.2 ± 0.43 day
were measured
Strain AzwK-3b and strain SD-21 degraded BPA in the absence of
-
1
(
exogenous Mn(II) in organic rich K-ASW-medium containing 2.0 g L
peptone and 0.5 g L-1 yeast extract (Fig. 1) (Learman et al., 2011).
Peptone and yeast extract are commonly used as carbon and nitrogen
sources as well as supplements to provide essential nutrients such as
-
1
-
1
1
.68 ± 0.37 day in the presence of 18 µM BPA and to 0.75 ± 0.23 day
in the presence of 44 µM BPA. The maximum growth yield as indicated
by OD600 nm measurements decreased by approximately 20% and 67%
vitamins and amino acids. Both peptone and yeast extract contain trace
metals, and Mn up to 3.2
μ
g g- (dry weight) has been reported for yeast
1
in the presence of 18 and 44 µM BPA, respectively. The addition of
1
00 µM Mn(II) relieved the inhibitory effect of BPA, and the growth
extract (Grant and Pramer, 1962). Indeed, ICP-MS determined that
K-ASW-medium contained 0.3 M Mn(II), suggesting that MnO2-bio--
yields recovered (Fig. S3), suggesting MnO2-bio-mediated BPA degrada-
tion alleviated the observed growth inhibition. Apparently, the forma-
tion of MnO2-bio protected strain AzwK-3b from BPA toxicity, and the
formation of MnO2-bio formation is a defense response to toxins sus-
μ
mediated BPA degradation could occur without exogenous Mn(II) sup-
ply. Additional experiments using Mn-free, defined mineral salt medium
with acetate as the sole carbon source (J-Acetate medium) still sup-
ported BPA degradation by strain AzwK-3b (Fig. S5). Mn(II) was not
detected in J-Acetate medium by ICP-MS (data not shown), indicating
2
ceptible to MnO -mediated oxidation and degradation. Indeed, Mn(II)
oxidation and MnO2-bio formation have been proposed to protect bac-
terial cells from toxic metals and reactive oxygen species (Tebo et al.,
co-metabolic BPA degradation rather than mediated by MnO
2
. The Mn
2
004; Ghiorse, 1984). For strain SD-21 and strain GB-1, no apparent
growth inhibition was observed with BPA concentrations up to 44 µM
Fig. S4a and b).
(II) detection limit as calculated by 3 /S, where is the standard de-
σ
σ
viation of five blank injections and S is the slope of the calibration curve
(Long and Winefordner, 1983), was 20.0 ± 4.4 nM. Strain SD-21 did not
grow in J-Acetate medium and the contribution of trace Mn(II) in yeast
extract on BPA degradation could not be examined; however, the high
BPA degradation rates observed in strain SD-21 cultures without Mn(II)
suggest that this bacterium can (co-)metabolize BPA (Fig. 1).
(
3
.4. BPA degradation intermediates
HCA has been detected as the major intermediate of BPA degradation
mediated by MnO2-syn (Lin et al., 2009; Im et al., 2015; Balgooyen et al.,
017, 2019). Because an in vitro estrogen receptor binding assay sug-
gested that HCA has a 100-fold higher binding affinity than BPA
Nakamura et al., 2011), the formation of HCA is of concern. In the
3
.6. BPA degradation in the absence of Mn
2
As of 2020, 24 genera, including Pseudomonas, have been reported to
(
harbor species capable of aerobic BPA degradation (Im and L o¨ ffler,
016; de Santana et al., 2019; Heidari et al., 2017), but BPA degradation
presence of Mn(II), HCA was detected as a degradation intermediate in
the cultures of all three bacterial species. BPA-to-HCA conversion effi-
2
has not been linked to the genera Roseobacter and Erythrobacter. When
Roseobacter sp. strain AzwK-3b and Erythrobacter sp. strain SD-21 were
ciency was calculated by dividing the amount ( mol) HCA formed by the
μ
amount BPA removed, assuming one mol of BPA will produce one mol of
HCA (Im et al., 2015). For strain AzwK-3b and strain GB-1, BPA-to-HCA
-
1
-1
incubated with 9
μ
M BPA (2 mg L ) and 18 M BPA (4 mg L ),
μ
respectively, in the absence of Mn(II), BPA was consumed (Fig. 2). In
strain AzwK-3b cultures, BPA consumption occurred at a rate of
conversion efficiencies were in
a
similar range to that of
-
1
0
.12 ± 0.04 day , but complete degradation was not achieved even
after an extended incubation period of 20 days (data not shown). Strain
SD-21 completely consumed 18 M BPA in 4 days at a rate of
.62 ± 0.28 day . Efforts to grow strain AzwK-3b and strain SD-21 in
defined mineral salt medium (Im et al., 2014b) with 9 and 18 M BPA as
μ
-
1
0
μ
the sole carbon source, respectively, were not successful and BPA was
not degraded (data not shown), suggesting that partial BPA consumption
observed in rich media was co-metabolic. For strain AzwK-3b, HCA was
detected during BPA degradation in the absence of Mn(II) (Fig. 6),
suggesting that this strain may have an oxidative pathway through
radical coupling, similar to MnO2-syn-mediated BPA degradation (Lin
et al., 2009). Enzymatic radical coupling has been proposed as a mi-
crobial co-metabolic degradation mechanism for pesticides (Bollag,
1
991) and lignin (Brown and Chang, 2014; Kirk and Farrell, 1987). In
Erythrobacter sp. strain SD-21 cultures, BPA was readily degraded in the
absence of Mn(II) but HCA was not detected (Fig. 6), suggesting that the
strain may have a different degradation pathway circumventing the
formation of HCA or the intermediate was readily turned over thereby
evading detection.
Fig. 6. Conversion efficiency of BPA to HCA in the absence or presence of Mn
II). The gray shaded area indicates the BPA-to-HCA conversion efficiency
(
Many aerobic bacteria and fungi possess genes encoding cytochrome
P450s. These heme-containing monooxygenase enzyme systems have
broad substrate specificity and attack on BPA has been documented
observed in MnO2-syn-mediated BPA degradation experiments reported previ-
ously (Im et al., 2015). Error bars represent the standard deviations of triplicate
samples of triplicate cultures.
5

N. Shobnam et al.
Journal of Hazardous Materials 417 (2021) 125987
(
Sasaki et al., 2005b; Kolvenbach et al., 2007). Metyrapone, a cyto-
Declaration of Competing Interest
chrome P450 inhibitor, is widely used to demonstrate the involvement
of cytochrome P450, and the addition of metyrapone repressed BPA
degradation activity in Sphingomonas sp. strain AO1 (Sasaki et al.,
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.
2
005a). Both strain AzwK-3b and strain SD-21 possess P450 genes, and
consumed some BPA without Mn(II) additions to the medium; however,
BPA consumption still occurred in the presence of metyrapone (Fig. S6)
suggesting that cytochrome P450 was not involved.
Acknowledgments
Many Pseudomonas isolates are known to aerobically degrade BPA
We thank Colleen Hansel (Woods Hole Oceanographic Institution,
MA) for providing Roseobacter sp. strain AzwK-3b, Bradley Tebo (Ore-
gon Health & Science University, OR) for providing Erythrobacter sp.
strain SD-21, and Hope A. Johnson (California State University, CA) for
providing Pseudomonas putida sp. strain GB-1. This work was supported
by the Polycarbonate/BPA Global Group of the American Chemistry
Council (ACC), Washington, DC.
Im and L o¨ ffler, 2016) and degradation rates as high as 82.9 day- have
1
(
been reported in P. monteilii strain N-502; (Masuda et al., 2007) how-
ever, no disappearance of BPA was observed in the incubations of
Pseudomonas putida strain GB-1. The inability of Pseudomonas putida
strain GB-1 to degrade BPA was unexpected because the strain has been
reported to possess cytochrome P450 enzyme systems (De Vrind et al.,
1
998). Further, many other Pseudomonas putida strains have been re-
ported to produce laccase and co-metabolize various organic com-
pounds, including BPA (Kuddus et al., 2013; Liu et al., 2016; Mandic
et al., 2019; Telke et al., 2009).
Appendix A. Supporting information
Supplementary data associated with this article can be found in the
online version at doi:10.1016/j.jhazmat.2021.125987.
Due to the hydrophobic nature of BPA (log Kow of 2.2–3.82) (Staples
et al., 1998), adsorption of BPA onto hydrophobic cell surface compo-
nents has been reported (Im et al., 2016; Endo et al., 2007). The OD600nm
in cultures of strain AzwK-3b, strain SD-21, and strain GB-1 that reached
early stationary phase in the absence of BPA were 0.096 ± 0.002,
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