Fate of Bisphenol A in Terrestrial and Aquatic ... - ACS Publications

Subscriber access provided by UNIV LAVAL

Critical Review

Fate of Bisphenol A in terrestrial and aquatic environments Jeongdae Im, and Frank E Löffler Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b00877 • Publication Date (Web): 12 Jul 2016 Downloaded from http://pubs.acs.org on July 13, 2016

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 44

Environmental Science & Technology

84x60mm (150 x 150 DPI)

ACS Paragon Plus Environment


1

Page 2 of 44

Fate of Bisphenol A in terrestrial and aquatic environments

2 Jeongdae Im1 and Frank E. Löffler2,3,4,5*

3 4 1

5

Department of Microbiology, University of Massachusetts,

6

Amherst, MA 01002, USA 2

7

Center for Environmental Biotechnology, University of Tennessee,

8

Knoxville, TN 37996 3

9

Department of Microbiology, University of Tennessee,

10


11

Department of Civil and Environmental Engineering, University of Tennessee,

12


13

University of Tennessee and Oak Ridge National Laboratory (UT-ORNL) Joint Institute for

14

Biological Sciences (JIBS) and Biosciences Division, Oak Ridge National Laboratory,

15

Oak Ridge, TN 37831

16 17

* Corresponding author

18

University of Tennessee

19

Department of Microbiology

20

M409 Walters Life Science Bldg.

21

Knoxville, TN 37996

22

Phone: +1-865-974-4933

23

Fax:

24

E-mail: [email protected]

+1-865-974-4007


1

Page 3 of 44


25

Abstract

26

Bisphenol A (2,2-bis[4-hydroxyphenyl]propane, BPA), the monomer used to produce

27

polycarbonate plastic and epoxy resins, is weakly estrogenic and therefore of environmental and

28

human health interest. Due to the high production volumes and disposal of products made from

29

BPA, polycarbonate plastic and epoxy resins, BPA has entered terrestrial and aquatic

30

environments. In the presence of oxygen, diverse taxa of bacteria, fungi, algae and even higher

31

plants metabolize BPA, but anaerobic microbial degradation has not been documented. Recent

32

reports demonstrated that abiotic processes mediate BPA transformation and mineralization in

33

the absence of oxygen, indicating that BPA is susceptible to degradation under anoxic

34

conditions. This review summarizes biological and non-biological processes that lead to BPA

35

transformation and degradation, and identifies research needs to advance predictive

36

understanding of the longevity of BPA and its transformation products in environmental systems.

37 38

Occurrence of BPA in the environment

39

Bisphenol A (2,2-bis[4-hydroxyphenyl]propane, BPA) is used in the plastics industry as a

40

monomer for producing polymeric materials, primarily epoxy resins, and polycarbonate plastic,

41

and is also used as a raw material for other products such as flame retardants.1–3 The global

42

demand of BPA exceeded 6.5 million tons in 2012 and is predicted to grow at an annual rate of

43

4.6% from 2013 to 2019.4 BPA products have permeated the daily lives of people in many ways.

44

For example, epoxy resins are used as dental sealants as well as internal protective coatings for

45

food cans, bottle tops and water pipes, while polycarbonate is used in a wide variety of common

46

products, including in digital media (e.g. CDs, DVDs), electronic equipment, automobiles, and

47

medical devices. Also, in thermal papers, free or non-polymerized BPA is used, where one side


2


Page 4 of 44

48

has a powdery layer of a thermally reactive coating containing BPA (up to 2.3% by weight),5 and

49

BPA contamination of recycled paper can occur.5,6 Due to the frequent and widespread use and

50

disposal of these products, BPA is released into the environment, mainly through processing of

51

BPA in manufacture, inefficient removal during wastewater treatment,7–10 landfill leachates,11–14

52

and leaching from discarded BPA-based materials (e.g., hydrolysis of polycarbonate, recycled

53

paper)5,15–17 (Figure 1). Consequently, BPA has been detected in various environmental systems

54

(Table 1), and, according to a recent survey, BPA and three other bisphenols have been detected

55

in human urine samples at high (up to 99%) frequency.18 Because of health concerns from

56

exposure to BPA,19–23 further evaluation of the environmental fate of BPA is warranted.

57

Currently, no data exist to support that BPA is produced naturally; however, there is evidence

58

that bisphenol F (BPF), which is structurally very similar to BPA and may have comparable

59

estrogenic potency24–26, is not a xenobiotic. For example, BPF and/or BPF derivatives were

60

detected in orchids27–29 and bamboo shoots.30 In addition, BPF concentration averaging 3.2 mg

61

kg-1 were measured in mild mustards made from Sinapis alba seeds.30 This is a remarkable

62

observation because mustard has been used as a condiment since Roman times31, and with an

63

average daily consumption of 1-2 g per person in the U.S. and Europe, the annual average BPF

64

intake via mustard was estimated to range between 1.2 and 2.4 mg per capita.30,32

65 66

Physicochemical properties of BPA

67

The reported aqueous phase solubility of BPA is 300 mg L-1 at 25 °C,33 with an octanol-water

68

partitioning coefficient (log Kow) of 3.42,34 and a Henry’s constant of 1.0

69

These parameters indicate that BPA is not volatile at ambient temperatures but has a high

70

tendency for sorption to soil and sediment.35–39 In addition, bound residue formation (i.e.,


10-10 atm m3 L-1.1

3

Page 5 of 44


71

incorporation of BPA into solid matrices involving covalent bonds) has been demonstrated.35,38

72

Therefore, desorption/release from soil and sediment may be a key factor controlling transport,

73

transformation, degradation and fate of BPA in the environment. The presence of heavy metals

74

and cationic surfactants can enhance desorption of BPA from soils,40 and complete desorption

75

can be accomplished, at least under laboratory conditions.40,41 Knowledge about the rates of BPA

76

desorption from a variety of matrices are largely unknown but obviously relevant because

77

aqueous phase BPA is more likely to be subject to natural attenuation including physical,

78

chemical, and biological processes that reduce contaminant toxicity.42,43

79 80

Scope

81

A PubMed search with the term “bisphenol A” (May 2016) identified more than 10,000

82

publications and reports investigating possible human health effects, and comprehensive review

83

articles discuss human exposure5,44,45 and toxicological aspects of BPA.3,19,20,46 Several national

84

health risk assessment reports are also available.21–23 This review does not discuss routes of

85

exposure to BPA and toxicological aspects. Rather, the aim is to assess the contributions of

86

biological and non-biological processes to BPA transformation and degradation in environmental

87

systems, and to summarize available process-specific information. Gaps in our understanding of

88

BPA degradation are identified with the goal to focus future research efforts and establish a

89

scientific basis for predicting the fate and longevity of BPA. Such information is needed to give

90

regulatory agencies the means for establishing meaningful maximum concentration level (MCL)

91

values and for informing the concerned public about possible exposure routes and realistic

92

dangers associated with environmental BPA. Figure 1 illustrates major sources and sinks of


4


93

environmental BPA, as well as recognized natural attenuation processes, which are the focus of

94

this review.

Page 6 of 44

95 96

Aerobic bacterial metabolism

97

Oxic conditions. In the presence of oxygen, BPA is susceptible to bacterial degradation, and

98

numerous bacterial isolates belonging to the α-Proteobacteria, β-Proteobacteria, γ-Proteobacteria,

99

Bacillus and Actinobacteria (Table 2) have been obtained and characterized. The first bacterial

100

isolate demonstrated to degrade BPA was Sphingomonas sp. strain MV1 isolated from sludge

101

collected from a wastewater treatment plant at a plastics manufacturing facility.47 Initially

102

defined as a coherent group of Gram-negative, strictly aerobic bacteria,48 the genus

103

Sphingomonas was later subdivided into the genera Sphingomonas, Sphingobium,

104

Novosphingobium, and Sphingopyxis within the family Sphingomonadaceae.49 The BPA-

105

degrading phenotype has been observed in all genera of this family,50–52 whose members

106

commonly occur in soil,53–56 freshwater,48 seawater,57 and wastewater47 habitats. As of 2015, 22 genera within the classes a-, b-, g-Proteobacteria, Bacilli, and

107 108

Actinobacteria have been reported to harbor members capable of metabolizing BPA under oxic

109

conditions (Table 2). Apparently, diverse bacterial groups inhabiting various environments share

110

the capability of metabolizing BPA in the presence of oxygen. Based on the identification of

111

BPA degradation intermediates, several pathways have been proposed. The major metabolic

112

routes proceed via oxidative skeletal rearrangement producing 4-isopropenylphenol (IPP), 4-

113

hydroxybenzaldehyde (HBAL), 4-hydroxybenzoate (HBA), 4-hydroxyacetophenone (HAP), 4-

114

hydroxycumyl alcohol (HCA) and hydroquinone (HQ), which represent the most frequently

115

observed BPA metabolites (Figure 2).47,58–60 IPP, HBAL, HBA, HAP, HCA, and HQ are


5

Page 7 of 44


116

mineralized and assimilated into cell carbon.47,58 An alternative, presumably minor route,

117

involves an initial hydroxylation step to produce 2,2-bis(4-hydroxyphenyl)-1-propanol, which is

118

further oxidized to HBA and 4-hydroxyphenacyl alcohol.47,58–61 The application of high-

119

resolution mass spectrometry techniques allowed the identification of other, presumably minor

120

intermediates62–65, and more complicated pathways that may contribute to BPA degradation have

121

been proposed.62–66

122

Bacterial genes and enzymes involved in aerobic BPA metabolism. Aerobic BPA

123

degradation pathways have been exhaustively studied, but relatively little is known about the

124

catalysts (i.e., enzymes) and the genes (Table 3). The addition of metyrapone, a cytochrome

125

P450 inhibitor, decreased BPA degradation activity of Sphingomonas sp. strain AO1.53

126

Subsequently, a cytochrome P450 monooxygenase system, consisting of cytochrome P450 and a

127

ferredoxin, was confirmed to be involved in BPA degradation using enzyme preparations of

128

strain AO1.54 Genome walking identified bisdA and bisdB genes encoding ferredoxin and

129

cytochrome P450, respectively, in strain AO1.67 Subsequently, Escherichia coli harboring a

130

bisdAB-recombinant plasmid was demonstrated to hydroxylate BPA, indicating that the bisdAB

131

genes were responsible for initiating BPA degradation in strain AO1.67 E. coli harboring only

132

bisdB also hydroxylated BPA, suggesting that native E. coli proteins fulfilled the ferredoxin

133

electron transfer function enabling cytochrome P450 activity in the E. coli mutant.67 Cytochrome

134

P450 monooxygenase was proposed to mediate an ipso substitution mechanism, whereby BPA is

135

initially hydroxylated at the ipso position to form a quinol intermediate.62–64 Following

136

rearomatization, the C-C bond between the semiquinol and the isopropylphenol moieties is

137

cleaved to produce hydroquinone and carbocationic isopropylphenol.63 More recently, BPA

138

metabolism in Sphingobium sp. strain BiD32 was investigated using quantitative proteomics and


6


Page 8 of 44

139

metabolomics.68 BPA-M (1,2-bis(4-hydroxyphenyl)-2-propanol) was proposed as the first

140

intermediate of BPA degradation.68 Among the proteins expressed in response to the presence of

141

BPA, a novel p-hydroxybenzoate hydroxylase was implicated in the initial BPA transformation

142

step and BPA-M formation.68 A putative cytochrome P450 encoded on the Sphingobium sp.

143

strain BiD32 genome was not detected; however, a ferredoxin, which is part of the cytochrome

144

P450 monooxygenase system, was measured. The ferredoxin was not differentially expressed in

145

response to BPA,68 suggesting that strain AO1 and strain BiD32 may use different BPA

146

degradation pathways. In summary, a number of bacterial species degrade BPA in the presence

147

of oxygen, suggesting that aerobic processes contribute to BPA attenuation in the

148

environment.1,66,69,70 Although some pathway information has emerged, additional efforts are

149

warranted to elucidate the genetic basis (i.e., genes), and the mechanisms (i.e., enzymes) that

150

govern bacterial BPA degradation in oxic environments.

151 152

Bacterial co-metabolism

153

The initial microbial transformation of BPA does not always lead to productive degradation, and

154

the benefits to the organisms are not apparent (i.e., co-metabolism). For example,

155

Mycobacterium sp. catalyzed O-methylation of BPA under oxic conditions, leading to the

156

formation of monomethyl- and dimethyl ethers (BPA-MME and BPA-DME, respectively)

157

(Figure 2).71 O-methylation diminished the affinity of BPA for the estrogen receptor,72 but

158

increased toxicity.71–73 Microbial degradation of BPA-MME and BPA-DME has not been

159

explored and the fate of these ether compounds is uncertain. The magnitude of O-methylation

160

activity is unknown and further investigations are needed to determine the occurrence and

161

environmental behavior of these methylated BPA transformation products.


7

Page 9 of 44


162

BPA disappearance was observed in Nitrosomonas europaea cultures expressing

163

ammonia monooxygenase (AMO), whereas no BPA loss was observed in control incubations

164

amended with allylthiourea, a potent inhibitor of AMO activity.74 Similar observations were

165

made in activated sludge incubations, and the BPA concentrations decreased concomitant with

166

ammonia oxidation, but ceased in the presence of allylthiourea.75 No reaction intermediates or

167

degradation end products were identified. An independent study identified nitro- and dinitro-

168

BPA in N. europaea cultures amended with BPA at pH 6.0, and cell-free incubation

169

demonstrated the abiotic nitration of BPA in the presence of nitrite (Figure 2).76 Hence, it is

170

currently unclear if AMO is directly involved in BPA transformation or if BPA reacts chemically

171

with the nitrite generated in the AMO reaction. The fate of nitrated bisphenols is currently

172

unclear but nitration apparently reduced estrogenic activity.76 Nitration was not observed at pH 7

173

and 8 suggesting this process may be limited to acidic conditions.

174

Methanotrophic bacteria possess soluble methane monooxygenase (sMMO) and

175

particulate methane monooxygenase (pMMO), both enzyme systems with broad substrate

176

specificities that fortuitously attacks an array of organic compounds.77–80 Methylosinus

177

trichosporium strain OB3b possesses both monooxygenases and serves as a model organism for

178

evaluating methanotrophic co-metabolism.81 Experiments with strain OB3b failed to demonstrate

179

BPA transformation under conditions conducive for sMMO and pMMO activity (Im et al.,

180

unpublished data). The current understanding of co-metabolic transformation potential of

181

bisphenols is limited, and additional testing of a broader diversity of ammonia-oxidizing and

182

methane-oxidizing microorganisms is warranted.

183 184

Some pseudomonads (e.g., Pseudomonas sp. strain LBC1) produce extracellular laccases capable of catalyzing BPA transformation reactions (Table 3).82 The strain LBC1 laccase


8


Page 10 of 44

185

efficiently degraded BPA even without redox mediators, which facilitate electron transfer and

186

can enhance laccase activity.82,83 These examples demonstrate that taxonomically diverse

187

bacteria expressing distinct enzyme systems that share broad range substrate specificity can co-

188

metabolize BPA under oxic conditions. Of note, BPA co-metabolism in the absence of oxygen

189

has not been reported and evidence for anaerobic co-metabolic transformation and degradation of

190

BPA is lacking.

191 192

Fungal transformation and degradation

193

Enzymes produced by ligninolytic fungi, including lignin peroxidase (LiP), manganese

194

peroxidases (MnP), versatile peroxidases (VP), and laccases are nonspecific, and therefore have

195

attracted attention for initiating degradation of many recalcitrant organic pollutants.83–88 Fungi

196

and fungal enzymes demonstrated to attack BPA are summarized in Table 3. The white-rot

197

basidiomycete Pleurotus ostreatus degraded BPA, and in vitro experiments demonstrated that

198

the organism’s MnP was involved in phenol, IPP, 4-isopropylphenol, and possibly hexestrol

199

formation (Figure 2).89 Similarly, MnPs produced by Phanerochaete chrysosporium and

200

Trametes versicolor quickly and completely removed BPA from the culture medium in

201

laboratory tests, and estrogenic activity declined with extended incubation times.90 These results

202

suggested that potential BPA transformation products with estrogenic activity were also

203

susceptible to MnP-mediated degradation.

204

In general, fungal laccases are less effective for BPA transformation and degradation than

205

MnP, but redox mediators can enhance their reactivity. For example, the presence of 1-

206

hydroxybenzotriazol,90,91 2,2-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid),92,93 or

207

acetosyringone93, fungal laccases demonstrated effective BPA transformation. The purified


9

Page 11 of 44


208

laccase from Trametes villosa transformed BPA to the mono-phenolic compound IPP and a BPA

209

dimer, suggesting that laccase activity may result in successive BPA polymerization.94 Similar

210

laccase-mediated BPA oligomerization was observed in cultures of the white rot fungus

211

Coriolopsis polyzona and BPA dimers, trimers, and tetramers were detected.92 The laccase of

212

Pycnoporus coccineus oxidized nonylphenol, octylphenol, and ethynylestradiol, but not BPA,95

213

indicating that not all fungal laccases initiate BPA transformation.

214 215

Algal BPA transformation

216

Microscopic, photosynthetic microalgae have been extensively investigated for bioremediation

217

applications as microalgae can sorb, accumulate, and/or metabolize a variety of contaminants.96

218

Under photoautotrophic conditions, Chlorella fusca and Anabaena variabilis removed 85% ± 7%

219

and 23% ± 6% of BPA, respectively, in 120 hours from aqueous solution containing 40 µM BPA

220

but no degradation products were detected (Hirooka et al., 2003).97 The microalgae

221

Nannochloropsis sp. and their zooplanktonic predators Artemia sp. and Brachionus sp. were

222

employed to investigate the possible accumulation of BPA along the food chain.98 These efforts

223

revealed that almost all BPA remained in the liquid medium when the zooplankton was

224

incubated alone. In contrast, 40% of the BPA was recovered from the zooplankton when

225

incubated together with the microalgae, suggesting BPA transfer and accumulation across

226

trophic levels.98 The major BPA transformation products formed by the green algae

227

Pseudokirchneriella subcapitata, Scenedesmus acutus, Scenedesmus quadricauda, Coelastrum

228

reticulatumwere, and Pavlova sp. were identified as BPA-glycosides, such as BPA-mono-O-b-D-

229

glucopyranoside and BPA-mono-O-b-D-galactopyranoside (Figure 2).99,100 Glycosylation of BPA

230

to non-estrogenic BPA-glycosides has also been observed in fungi and plants, presumably as


10


Page 12 of 44

231

intermediates of a detoxification process.99–106 Although BPA-glycosides do not have estrogenic

232

activity, hydrolases (i.e., b-glucosidase) can release BPA in the mammalian intestine.99 To date,

233

no BPA degradation intermediates have been reported as a consequence of algal metabolism, at

234

least in axenic cultures. Recently, symbiotic (i.e., commensal) BPA degradation was reported

235

and the microalgae Chlorella sorokiniana provided oxygen to a BPA-degrading bacterial mixed

236

culture.107

237 238

Phyto-transformation and degradation of BPA

239

In phytoremediation, green plants transform, stabilize, and remove inorganic and organic

240

contaminants from soil and water.108 Several plant species have been investigated for their ability

241

to remove BPA.102–104,109–121 Three main BPA metabolic pathways were observed in plants and

242

plant extracts: (i) conjugation with soluble carbohydrates (glycosylation), (ii) formation of bound

243

residues, and (iii) formation of polar polymers.100,102,104,110,111 Among these pathways, BPA

244

glycosylation is regarded as the main metabolic route of BPA in plants. For example, Nicotiana

245

tabacum cell suspensions102 and Ipomoea aquatica (water spinach)104 absorbed and metabolized

246

BPA to BPA-mono-O-b-D-glucopyranoside as a major product, and several other BPA-

247

glycosides were detected in Eucalyptus perriniana cell suspension cultures (Figure 2).111 The

248

fate of these BPA adducts is unclear and it is possible that BPA-glycoside hydrolysis releases

249

BPA.99 Therefore, further investigations of BPA metabolites in edible plants are warranted. A

250

few studies demonstrated BPA degradation associated with plant metabolism, and monophenols,

251

such as IPP and HCA, were reported as BPA metabolites in addition to monohydroxyl BPA and

252

BPA-glycosides (Figure 2).111,117 Oxidative enzymes, such as peroxidases and polyphenol


11

Page 13 of 44


253

oxidases, have been implicated in the ring cleavage reactions118–122 (Table 3) suggesting that

254

BPA degradation in plants could potentially occur.

255 256

BPA degradation under anoxic conditions

257

Information about microbial BPA degradation in the absence of oxygen is scarce, and several

258

studies have concluded that BPA is recalcitrant to anaerobic microbial (co-) metabolism.37,39,123–

259

126

260

1).127,128 No microbial BPA degradation was observed in anoxic microcosms established with

261

freshwater sediment,36,39,124,125,129 marine sediments,126 and soil,37 leading to the conclusion that

262

BPA is recalcitrant and undergoes little or no biodegradation in the absence of oxygen.

263

Reductive dehalogenation of halogenated BPA derivatives occurred in estuarine sediment

264

microcosms, but no further degradation was observed under anoxic conditions.125,130–135

265

Contrasting these observations, a BPA half-life of less than 1 day was reported in denitrifying

266

columns established with aquifer material.136 BPA disappearance was also reported under

267

sulfate-, nitrate-, and iron-reducing conditions established in microcosms derived from

268

freshwater sediment.137 Experiments with Bacillus sp. strain GZB, a facultative anaerobe,

269

suggested BPA removal under both oxic and anoxic conditions.138 Although these studies

270

demonstrated BPA disappearance, BPA transformation/degradation products were not measured

271

and quantified, and BPA degradation in the absence of oxygen has yet to be demonstrated. Ten

272

strains of Lactococcus (four L. lactis subsp. lactis, five L. lactis subsp. lactis bv. diacetylactis,

273

and one L. lactis subsp. cremoris) were examined for their ability to remove BPA from aqueous

274

solution under anoxic conditions.139 While the aqueous phase BPA concentrations decreased by

275

9-62% in live incubations, no degradation products were detected. An independent study

This is of interest because a substantial mass of BPA resides in anoxic sediments (Table


12


Page 14 of 44

276

reported BPA concentration decreases of 20% in E. coli cultures unable to degrade BPA.140

277

Additional experiments revealed that BPA adsorption to the biomass, rather than

278

transformation/degradation, explained BPA disappearance.139,140 These are relevant observations

279

indicating that BPA disappearance is a poor indicator of degradation and experimental data

280

documenting a decrease in BPA concentrations must be carefully interpreted. Taken together,

281

unequivocal evidence demonstrating metabolic and co-metabolic microbial BPA degradation in

282

the absence of oxygen is currently lacking.

283 284

Abiotic BPA transformation and degradation

285

A number of abiotic processes can lead to BPA transformation and degradation. While processes

286

involving reactive oxygen species (ROS) are generally limited to oxic environments, reactive

287

mineral phases can mediate BPA degradation under oxic and anoxic conditions.

288

Photo-degradation. BPA is susceptible to light-induced transformation. In photolysis (photo-

289

oxidation), photons initiate a chemical breakdown process, which represents an important

290

transformation pathway for many organic pollutants in surface waters and surface soils.141,142

291

BPA half-lifes in surface waters ranged from 66 hours to 160 days and the efficiency of

292

photolytic degradation depended on pH, turbidity, water turbulence and other factors.143 BPA

293

photo-degradation intermediates include phenol, 4-isopropylphenol and a semi-quinone

294

derivative of BPA.143

295

Photo-oxidation, also known as indirect photolysis, refers to the degradation of a

296

compound by naturally occurring ROS including hydroxyl radicals (OH•), peroxide radicals

297

(ROO•) and singlet oxygen (1O2) generated by light. For example, in the presence of nitrite or

298

nitrate, solar radiation can induce the formation of hydroxyl radicals from water,144 and the


13

Page 15 of 44


299

subsequent ROS-mediated transformation of BPA has been demonstrated.145,146 In the presence

300

of ROS, NaCl enhanced BPA degradation by producing reactive hypochlorite (OCl-).15

301

Dissolved organic matter,145,147,148 ferric iron,145,149 lipids,150 and riboflavin151,152 have also been

302

implicated in ROS formation and BPA transformation.

303

Advanced oxidation. BPA concentrations in wastewater effluent range from low ppb to several

304

ppm levels (Table 1). Many studies demonstrated the utility of advanced oxidation (AO)

305

processes based on H2O2- (e.g., Fenton chemistry), UV light-, and ozone-enabled removal of

306

BPA in aquatic compartments. The interested reader is referred to review articles describing AO

307

processes in detail.10,153–157 AO processes can effectively remove BPA in engineered systems

308

(e.g., wastewater treatment plants), and possibly expanded for enhanced treatment of

309

contaminants in aquifers and sediments. A recent study demonstrated that Shewanella oneidensis

310

mediated Fenton chemistry-based degradation of 1,4-dioxane when the culture was provided

311

with a suitable electron donor (lactate) and ferric iron as an electron acceptor, and was exposed

312

to alternating oxic-anoxic conditions.158 This observation suggests that microbially mediated

313

Fenton chemistry can potentially contribute to contaminant degradation at circumneutral pH near

314

oxic-anoxic interfaces.

315

Zero-valent iron (ZVI). ZVI is reactive towards a variety of organic compounds.159 The ZVI-

316

mediated production of hydroxyl radicals was implicated in BPA degradation, but no

317

transformation products were reported.160 Similarly, degradation of aqueous phase BPA using

318

nano-sized ZVI in the presence of hydrogen peroxide and persulfate oxidants has been

319

demonstrated.161

320

Reactive mineral phases. Manganese and iron can form reactive mineral phases that affect the

321

fate and transport of organic contaminants via sorption, hydrolysis and/or oxidative


14


322

transformation. In particular, manganese oxides are strong, naturally occurring oxidants, and

323

play relevant roles in the biogeochemical cycling of carbon and other elements.162–164 Recent

324

studies demonstrated that manganese dioxide (MnO2)165–168 mediates BPA transformation.

325

Page 16 of 44

As a strong oxidant, MnO2 serves as an electron acceptor in microbial respiration under

326

anoxic conditions and also as a mineral phase reactive towards many organic contaminants.165–171

327

Oxidative transformation of BPA by MnO2 has been demonstrated using synthetic MnO2,165–168

328

and several transformation pathways were suggested based on the identification of reaction

329

intermediates.165 A proposed initial electron transfer step to MnO2 results in the formation of

330

BPA radicals, which subsequently undergo a variety of reactions (Figure 2).165 HCA was

331

identified as a major transformation intermediate, and at least 64% (mol/mol) of the initial

332

amount of BPA was recovered as HCA (Figure 2).168 HCA was also susceptible to MnO2-

333

mediated degradation and mineralization (i.e., CO2 evolution) occurred, indicating that complete

334

destruction of BPA can be achieved in the reaction with MnO2 in the absence of oxygen, at least

335

under laboratory conditions.168 Compared to BPA, HCA has an octanol-water partition

336

coefficient (Log Kow) of 0.76 (BPA 2.76) and an aqueous phase solubility of 2.65 g L-1 (BPA

337

0.31 g L-1).168 The different physicochemical properties suggest that HCA has increased mobility

338

in water-saturated systems compared to BPA, and is therefore more likely to encounter oxic

339

zones. HCA appears recalcitrant to microbial degradation under anoxic conditions, but is rapidly

340

utilized as a growth substrate in the presence of oxygen.168 Recently, the utility of MnO2 as an

341

additive to engineered stormwater infiltration systems to oxidize organic contaminants, including

342

BPA, was demonstrated.172 Goethite also has been reported to mediate degradation of certain organic pollutants,173,174

343 344

and oxidative transformation of BPA has been observed in aqueous suspensions of goethite (a-


15

Page 17 of 44


345

FeOOH).175 Transformation reactions similar to those observed in MnO2-mediated BPA

346

degradation were proposed,175 but HCA was not detected, suggesting that the goethite-mediated

347

BPA degradation pathway differs.

348

Goethite is a common and thermodynamically stable iron oxide in soils,176 and

349

manganese oxides occur widely in freshwater and marine sediments. For example, 25 to 185

350

µmol mL-1 of MnO2 have been detected in marine sediments,177 and even greater amounts of 300

351

- 4,000 µmol mL-1 of MnO2 have been observed in freshwater sediments.178,179 The amounts of

352

MnO2 observed in natural soils and sediments are in the range of nominal MnO2 concentrations

353

used in laboratory experiments that demonstrated MnO2-mediated BPA mineralization.168 Of

354

course, many factors including pH, dissolved organic matter, metal ion concentrations, microbial

355

activity, etc., influence mineral phase formation, reactivity, and passivation165,180–182 and the

356

contributions of reactive mineral phases to BPA degradation in environmental systems have yet

357

to be evaluated. A relevant aspect that is poorly understood is the interplay between biotic and

358

abiotic reactions. Ferrous iron- and manganic ion-oxidizing microbes play key roles in

359

generating the reactive mineral phases, and more detailed studies of biologically mediated

360

abiotic degradation (BMAD) processes (e.g., microbial Mn2+ oxidation and mineral phase

361

formation followed by MnO2-mediated BPA degradation) are needed. It is conceivable that such

362

BMAD processes have major contributions for in situ BPA attenuation and for controlling the

363

fate and longevity of BPA in sediments and aquifers.

364 365

Bound residue formation

366

Many hydrophobic organic compounds and their transformation products form non-extractable

367

bound residues in soils,183 and this process has been considered a major attenuation pathway.184


16


Page 18 of 44

368

Bound residue formation of BPA into the soil matrix has been demonstrated under oxic

369

conditions, and the portion of the bound residue increased significantly as a function of time,35,38

370

and microbial activity has been implicated in bound residue formation.38,185,186 On the other

371

hand, a substantial amount of tetrabromobisphenol A (TBBPA) incorporated into the soil matrix

372

under anoxic conditions, but was released upon exposure to oxygen.38 The release of

373

contaminants covalently incorporated into the biomass has been reported in response to changing

374

physicochemical conditions and microbial activity.186,187 For example, a change in soil redox

375

conditions can impact the structure of natural organic matter (NOM), which affects the binding

376

and sorption of organic pollutants to NOM.38,188

377

Bound residue formation decreases the risk of exposure, but at the same time decreases

378

contaminant availability for biotic and abiotic degradation. There is an ongoing debate regarding

379

whether bound residues of organic compounds remain (bio)available in the long term.187,189

380

Further studies on the stability of bound residues of BPA in soils or sediments under dynamic

381

environmental conditions are warranted.

382 383

Knowledge gaps

384

BPA and BPA derivatives are, and will remain, part of modern societies for decades to come,

385

and so will the associated concerns, unless research provides clear understanding about the fate

386

and the longevity of bisphenols in environmental systems. As outlined above, a variety of biotic

387

and abiotic processes that contribute to BPA transformation, degradation, and incorporation into

388

solid matrices (e.g., soil, sediment) have been identified and documented in the laboratory. Still,

389

many open questions about the ultimate fate of BPA and its metabolites in environmental

390

systems remain, and more information about degradation pathways and mechanisms, cornerstone


17

Page 19 of 44


391

organisms, enzymes and genes, as well as favorable geochemical conditions that sustain

392

acceptable degradation rates is needed. The biogeochemical settings conducive for BPA

393

degradation and detoxification must be better delineated, and tools to quantitatively assess BPA

394

transformation/degradation processes are desirable. Under anoxic conditions, mineral phase-

395

mediated reactivity is relevant but the turnover and formation of the reactive minerals (e.g.,

396

MnO2) are not fully characterized, making predictive understanding of the contributions of

397

abiotic degradation tenuous. Most knowledge about the fate of BPA has accrued from

398

laboratory-based studies but comprehensive efforts to explore the relative contributions of

399

different attenuation mechanisms under in situ conditions are lacking.

400 401

Perspective on the fate of BPA in terrestrial and aquatic environmental systems

402

Identification of the major BPA sources is a key first step for addressing the concerns associated

403

with BPA. Among the sources of environmental BPA shown in Figure 1, permitted wastewater

404

effluent discharge is considered the main entry way for BPA into terrestrial and aquatic

405

environments.190,191 As outlined in this review, a substantial body of knowledge has accrued

406

about biotic and abiotic BPA transformation/degradation processes and pathways in laboratory

407

studies. Table 4 summarizes the reported processes and the associated rates leading to BPA

408

removal. Interestingly, the degradation/transformation rates observed in laboratory studies using

409

bacteria, fungi, algae and plants are in a similar range, and in situ studies are needed to decipher

410

the relative contributions of the different processes for BPA decomposition under

411

environmentally relevant conditions. Of note, these processes require oxygen, and under anoxic

412

conditions, BPA transformation/degradation appears to be limited to reactions with reactive

413

mineral phases. Laboratory studies reveal that MnO2-mediated BPA degradation occurs at


18


Page 20 of 44

414

several orders of magnitude higher rates than those reported for other processes (Table 4).

415

Considering that a major concern is BPA associated with (anoxic) sediment, Mn-cycling near

416

oxic-anoxic interfaces may be a major process controlling the fate of BPA in sediments. Based

417

on the current understanding of processes leading to BPA removal, engineering solutions at the

418

identified key points of entry could be envisaged to eliminate further release of BPA into the

419

environment. The information obtained from laboratory studies indicates that BPA is susceptible

420

to natural attenuation processes under oxic and anoxic conditions, and an important next step

421

will be to assess the relevance of the different potential attenuation processes on environmental

422

BPA concentrations. Understanding of BPA transformation and degradation has advanced to a

423

level that justifies integrated in situ studies that consider all known BPA attenuation

424

mechanisms. Comprehensive in situ efforts can evaluate the environmental fate of BPA and

425

reveal realistic exposure routes, so that potential dangers to human and environmental health can

426

be clearly delineated and predicted.

427 428

Acknowledgements

429

This work was supported by the Polycarbonate/BPA Global Group of the American Chemistry

430

Council (ACC), Washington, DC, USA.

431 432

References

433 434 435 436 437 438 439 440

(1)

(2)

(3)

Staples, C. A.; Dome, P. B.; Klecka, G. M.; Sandra, O. T.; Harris, L. R. A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 1998, 36 (10), 2149–2173. Crain, D. A.; Eriksen, M.; Iguchi, T.; Jobling, S.; Laufer, H.; LeBlanc, G. A.; Guillette, L. J. An ecological assessment of bisphenol-A: Evidence from comparative biology. Reprod. Toxicol. 2007, 24 (2), 225–239. Rochester, J. R. Bisphenol A and human health: A review of the literature. Reprod. Toxicol. 2013, 42, 132–155.


19

Page 21 of 44

441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483


(4)

(5)

(6) (7)

(8)

(9)

(10) (11) (12)

(13) (14)

(15) (16)

(17)

(18)

(19)

Transparency Market Research. Bisphenol A market for polycarbonates, epoxy resins and other applications - global industry analysis, aize, share, growth and forecast, 2013 2019; 2013. Geens, T.; Aerts, D.; Berthot, C.; Bourguignon, J. P.; Goeyens, L.; Lecomte, P.; MaghuinRogister, G.; Pironnet, A. M.; Pussemier, L.; Scippo, M. L.; et al. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem. Toxicol. 2012, 50 (10), 3725–3740. Mendum, T.; Stoler, E.; VanBenschoten, H.; Warner, J. C. Concentration of bisphenol A in thermal paper. Green Chem. Lett. Rev. 2011, 4 (1), 81–86. Lee, H. B.; Peart, T. E. Determination of bisphenol A in sewage effluent and sludge by solid-phase and supercritical fluid extraction and gas chromatography/mass spectrometry. J. AOAC Int. 2000, 83 (2), 290–297. Fromme, H.; Küchler, T.; Otto, T.; Pilz, K.; Müller, J.; Wenzel, A. Occurrence of phthalates and bisphenol A and F in the environment. Water Res. 2002, 36 (6), 1429– 1438. Robinson, B. J.; Hui, J. P. M.; Soo, E. C.; Hellou, J. Estrogenic compounds in seawater and sediment from Halifax Harbour, Nova Scotia, Canada. Environ. Toxicol. Chem. 2009, 28 (1), 18–25. Melcer, H.; Klečka, G. Treatment of wastewaters containing Bisphenol A: State of the science review. Water Environ. Res. 2011, 83 (7), 650–666. Yamamoto, T.; Yasuhara, A.; Shiraishi, H.; Nakasugi, O. Bisphenol A in hazardous waste landfill leachates. Chemosphere 2001, 42 (4), 415–418. Schwarzbauer, J.; Heim, S.; Brinker, S.; Littke, R. Occurrence and alteration of organic contaminants in seepage and leakage water from a waste deposit landfill. Water Res. 2002, 36 (9), 2275–2287. Arp, H. P. H. Compilation of Norwegian screening data for selected contaminants (2002 – 2012); 2012. Kalmykova, Y.; Björklund, K.; Strömvall, A. M.; Blom, L. Partitioning of polycyclic aromatic hydrocarbons, alkylphenols, bisphenol A and phthalates in landfill leachates and stormwater. Water Res. 2013, 47 (3), 1317–1328. Sajiki, J.; Yonekubo, J. Leaching of bisphenol A (BPA) to seawater from polycarbonate plastic and its degradation by reactive oxygen species. Chemosphere 2003, 51 (1), 55–62. Teuten, E. L.; Saquing, J. M.; Knappe, D. R. U.; Barlaz, M. A.; Jonsson, S.; Björn, A.; Rowland, S. J.; Thompson, R. C.; Galloway, T. S.; Yamashita, R.; et al. Transport and release of chemicals from plastics to the environment and to wildlife. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2009, 364 (1526), 2027–2045. Hirai, H.; Takada, H.; Ogata, Y.; Yamashita, R.; Mizukawa, K.; Saha, M.; Kwan, C.; Moore, C.; Gray, H.; Laursen, D.; et al. Organic micropollutants in marine plastics debris from the open ocean and remote and urban beaches. Mar. Pollut. Bull. 2011, 62 (8), 1683– 1692. Ye, X.; Wong, L.-Y.; Kramer, J.; Zhou, X.; Jia, T.; Calafat, A. M. Urinary concentrations of Bisphenol A and three other Bisphenols in convenience samples of U.S. adults during 2000–2014. Environ. Sci. Technol. 2015, 49 (19), 11834–11839. Sekizawa, J. Low-dose effects of bisphenol A: A serious threat to human health? J.


20


484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526

(20)

(21) (22) (23) (24)

(25)

(26)

(27) (28)

(29) (30)

(31) (32) (33)

(34)

(35)

Page 22 of 44

Toxicol. Sci. 2008, 33 (4), 389–403. Hengstler, J. G.; Foth, H.; Gebel, T.; Kramer, P.-J.; Lilienblum, W.; Schweinfurth, H.; Völkel, W.; Wollin, K.-M.; Gundert-Remy, U. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol A. Crit. Rev. Toxicol. 2011, 41 (4), 263– 291. European Food Safety Authority. Report on the two-phase public consultation on the draft EFSA scientific opinion on bisphenol A; Parma, Italy, 2015. National Toxicology Program. Monograph on the potential human reproductive and developmental effects of bisphenol A; Research Triangle Park, NC, 2008. Bureau of Chemical Safety. Health risk assessment of bisphenol A from food packaging applications; 2008. Eladak, S.; Grisin, T.; Moison, D.; Guerquin, M. J.; N’Tumba-Byn, T.; Pozzi-Gaudin, S.; Benachi, A.; Livera, G.; Rouiller-Fabre, V.; Habert, R. A new chapter in the bisphenol a story: Bisphenol S and bisphenol F are not safe alternatives to this compound. Fertil. Steril. 2015, 103 (1), 11–21. Rochester, J. R.; Bolden, A. L. Bisphenol S and F: A systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ. Health Perspect. 2015, 123 (7), 643–650. Chen, D.; Kannan, K.; Tan, H.; Zheng, Z.; Feng, Y.-L.; Wu, Y.; Widelka, M. Bisphenol analogues other than BPA: Environmental occurrence, human exposure, and toxicity – A review. Environ. Sci. Technol. 2016, acs.est.5b05387. Yi-Ming, L.; Zhuo-Lun, Z.; Yong-Fu, H. New phenolic derivatives from Galeola faberi. Planta Med. 1993, 59 (04), 363–365. Huang, S.-Y.; Li, G.-Q.; Shi, J.-G.; Mo, S.-Y.; Wang, S.-J.; Yang, Y.-C. Chemical constituents of the rhizomes of Coeloglossum viride var. bracteatum. J. Asian Nat. Prod. Res. 2004, 6 (1), 49–61. Zhang, Z.-C.; Su, G.; Li, J.; Wu, H.; Xie, X.-D. Two new neuroprotective phenolic compounds from Gastrodia elata. J. Asian Nat. Prod. Res. 2013, 15 (6), 619–623. Zoller, O.; Brüschweiler, B. J.; Magnin, R.; Reinhard, H.; Rhyn, P.; Rupp, H.; Zeltner, S.; Felleisen, R. Natural occurrence of bisphenol F in mustard. Food Addit. Contam. Part A 2015, 49, 1–10. Vaughan, J. G.; Hemingway, J. S. The utilization of mustards. Econ. Bot. 1959, 13 (3), 196–204. R. Dietrich, D.; Hengstler, J. G. From bisphenol A to bisphenol F and a ban of mustard due to chronic low-dose exposures? Arch. Toxicol. 2016, 90 (2), 489–491. Shareef, A.; Angove, M. J.; Wells, J. D.; Johnson, B. B. Aqueous solubilities of estrone, 17β-estradiol, 17α-ethynylestradiol, and bisphenol A. J. Chem. Eng. Data 2006, 51 (3), 879–881. Borrirukwisitsak, S.; Keenan, H. E.; Gauchotte-Lindsay, C. Effects of salinity, pH and temperature on the octanol-water partition coefficient of Bisphenol A. Int. J. Environ. Sci. Dev. 2012, 3 (5), 460–464. Fent, G.; Hein, W. J.; Moendel, M. J.; Kubiak, R. Fate of 14C-bisphenol A in soils. Chemosphere 2003, 51 (8), 735–746.


21

Page 23 of 44

527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569


(36) (37) (38)

(39)

(40) (41)

(42) (43)

(44) (45)

(46)

(47)

(48)

(49)

(50)

Ying, G.-G.; Kookana, R. S.; Dillon, P. Sorption and degradation of selected five endocrine disrupting chemicals in aquifer material. Water Res. 2003, 37 (15), 3785–3791. Ying, G.-G.; Kookana, R. S. Sorption and degradation of estrogen-like-endocrine disrupting chemicals in soil. Environ. Toxicol. Chem. 2005, 24 (10), 2640–2645. Liu, J.; Wang, Y.; Jiang, B.; Wang, L.; Chen, J.; Guo, H.; Ji, R. Degradation, metabolism, and bound-residue formation and release of tetrabromobisphenol A in soil during sequential anoxic–oxic incubation. Environ. Sci. Technol. 2013, 47 (15), 8348−8354. Im, J.; Prevatte, C. W.; Lee, H. G.; Campagna, S. R.; Löffler, F. E. 4-Methylphenol produced in freshwater sediment microcosms is not a bisphenol A metabolite. Chemosphere 2014, 117C, 521–526. Li, J.; Zhou, B.; Liu, Y.; Yang, Q.; Cai, W. Influence of the coexisting contaminants on bisphenol A sorption and desorption in soil. J. Hazard. Mater. 2008, 151 (2-3), 389–393. Loffredo, E.; Senesi, N. Fate of anthropogenic organic pollutants in soils with emphasis on adsorption/desorption processes of endocrine disruptor compounds. Pure Appl. Chem. 2006, 78 (5), 947–961. USEPA. Monitored natural attenuation of petroleum Hydrocarbons; Ada, OK, 1999. Alvarez, P. J. J.; Illman, W. A. Bioremediation and natural attenuation: Process fundamentals and mathematical models; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2005. Vandenberg, L. N.; Hauser, R.; Marcus, M.; Olea, N.; Welshons, W. V. Human exposure to bisphenol A (BPA). Reprod. Toxicol. 2007, 24 (2), 139–177. Calafat, A. M.; Ye, X.; Wong, L. Y.; Reidy, J. A.; Needham, L. L. Exposure of the U.S. population to Bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ. Health Perspect. 2008, 116 (1), 39–44. Peretz, J.; Vrooman, L.; Ricke, W. A.; Hunt, P. A.; Ehrlich, S.; Hauser, R.; Padmanabhan, V.; Taylor, H. S.; Swan, S. H.; Vandevoort, C. A.; et al. Bisphenol A and reproductive health: Update of experimental and human evidence, 2007-2013. Environ. Health Perspect. 2014, 122 (8), 775–786. Lobos, J. H.; Leib, T. K.; Su, T. M. Biodegradation of bisphenol A and other bisphenols by a gram-negative aerobic bacterium. Appl. Environ. Microbiol. 1992, 58 (6), 1823– 1831. Yabuuchi, E.; Yano, I.; Oyaizu, H.; Hashimoto, Y.; Ezaki, T.; Yamamoto, H. Proposals of Sphingomonas paucimobilis gen. nov. and comb. nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb. nov., and two genospecies of the genus Sphingomonas. Microbiol. Immunol. 1990, 34 (2), 99–119. Takeuchi, M.; Hamana, K.; Hiraishi, A. Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int. J. Syst. Evol. Microbiol. 2001, 51 (4), 1405–1417. Yamanaka, H.; Moriyoshi, K.; Ohmoto, T.; Ohe, T.; Sakai, K. Efficient microbial degradation of bisphenol A in the presence of activated carbon. J. Biosci. Bioeng. 2008, 105 (2), 157–160.


22


570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612

(51)

(52)

(53)

(54)

(55)

(56)

(57)

(58) (59)

(60)

(61) (62)

(63)

(64)

(65)

Page 24 of 44

Toyama, T.; Sato, Y.; Inoue, D.; Sei, K.; Chang, Y. C.; Kikuchi, S.; Ike, M. Biodegradation of bisphenol A and bisphenol F in the rhizosphere sediment of Phragmites australis. J. Biosci. Bioeng. 2009, 108 (2), 147–150. Zhou, N. A.; Lutovsky, A. C.; Andaker, G. L.; Gough, H. L.; Ferguson, J. F. Cultivation and characterization of bacterial isolates capable of degrading pharmaceutical and personal care products for improved removal in activated sludge wastewater treatment. Biodegradation 2013, 24 (6), 813–827. Sasaki, M.; Maki, J.; Oshiman, K.; Matsumura, Y.; Tsuchido, T. Biodegradation of bisphenol A by cells and cell lysate from Sphingomonas sp. strain AO1. Biodegradation 2005, 16 (5), 449–459. Sasaki, M.; Akahira, A.; Oshiman, K. I.; Tsuchido, T.; Matsumura, Y. Purification of cytochrome P450 and ferredoxin, involved in bisphenol A degradation, from Sphingomonas sp. strain AO1. Appl. Environ. Microbiol. 2005, 71 (12), 8024–8030. Oshiman, K.; Tsutsumi, Y.; Nishida, T.; Matsumura, Y. Isolation and characterization of a novel bacterium, Sphingomonas bisphenolicum strain AO1, that degrades bisphenol A. Biodegradation 2007, 18 (2), 247–255. Matsumura, Y.; Chiemi, H.; Miho, S.-M.; Ayako, A.; Fukunaga, K.; Toshihiko, I.; Oshiman, K.-I.; Tsuchido, T. Isolation and characterization of novel bisphenol Adegrading bacteria from soils. Biocontrol Sci. 2009, 14 (4), 161–169. Sakai, K.; Yamanaka, H.; Moriyoshi, K.; Ohmoto, T.; Ohe, T. Biodegradation of bisphenol A and related compounds by Sphingomonas sp. strain BP-7 isolated from seawater. Biosci. Biotechnol. Biochem. 2007, 71 (1), 51–57. Spivacks, J.; Leib, T. K.; Lobos, J. H. Novel pathway for bacterial metabolism of bisphenol A. Biochemistry 1994, 269 (10), 7323–7329. Ike, M.; Jin, C.-S.; Fujita, M. Isolation and characterization of a novel bisphenol Adegrading bacterium Pseudomonas paucimobilis strain FJ-4. Japanese Journal of Water Treatment Biology. 1995, pp 203–212. Suzuki, T.; Nakagawa, Y.; Takano, I.; Yaguchi, K.; Yasuda, K. Environmental fate of bisphenol A and its biological metabolites in river water and their xeno-estrogenic activity. Environ. Sci. Technol. 2004, 38 (8), 2389–2396. Ike, M.; Jin, C. S.; Fujita, M. Biodegradation of bisphenol A in the aquatic environment. Water Sci. Technol. 2000, 42 (7-8), 31–38. Gabriel, F. L. P.; Cyris, M.; Giger, W.; Kohler, H. P. E. ipso-substitution: A general biochemical and biodegradation mechanism to cleave α-quaternary alkylphenols and bisphenol A. Chem. Biodivers. 2007, 4 (9), 2123–2137. Kolvenbach, B.; Schlaich, N.; Raoui, Z.; Prell, J.; Zühlke, S.; Schäffer, A.; Guengerich, F. P.; Corvini, P. F. X. Degradation pathway of bisphenol A: Does ipso substitution apply to phenols containing a quaternary α-carbon structure in the para position? Appl. Environ. Microbiol. 2007, 73 (15), 4776–4784. Kohler, H.-P. E.; Gabriel, F. L. P.; Giger, W. ipso substitution – A novel pathway for microbial metabolism of endocrine-disrupting 4-nonylphenols, 4-alkoxyphenols, and Bisphenol A. Chim. Int. J. Chem. 2008, 62 (5), 358–363. Fischer, J.; Kappelmeyer, U.; Kastner, M.; Schauer, F.; Heipieper, H. J. The degradation


23

Page 25 of 44

613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655


(66) (67)

(68)

(69) (70)

(71)

(72)

(73)

(74)

(75)

(76)

(77)

(78) (79)

of bisphenol A by the newly isolated bacterium Cupriavidus basilensis JF1 can be enhanced by biostimulation with phenol. Int. Biodeterior. Biodegradation 2010, 64 (4), 324–330. Zhang, W.; Yin, K.; Chen, L. Bacteria-mediated bisphenol A degradation. Appl. Microbiol. Biotechnol. 2013, 97 (13), 5681–5689. Sasaki, M.; Tsuchido, T.; Matsumura, Y. Molecular cloning and characterization of cytochrome P450 and ferredoxin genes involved in bisphenol a degradation in Sphingomonas bisphenolicum strain AO1. J. Appl. Microbiol. 2008, 105 (4), 1158–1169. Zhou, N. A.; Kjeldal, H.; Gough, H. L.; Nielsen, J. L. Identification of putative genes involved in Bisphenol A degradation using differential protein abundance analysis of Sphingobium sp. BiD32. Environ. Sci. Technol. 2015, 49 (20), 12231–12241. Dorn, P. B.; Chou, C.; Gentempo, J. J. Degradation of bisphenol A in natural waters. Chemosphere. 1987, pp 1501–1507. Klecka, G. M.; Gonsior, S. J.; West, R. J.; Goodwin, P. A.; Markham, D. A. Biodegradation of bisphenol A in aquatic environments: River die-away. Environ. Toxicol. Chem. 2001, 20 (12), 2725–2735. McCormick, J. M.; Van Es, T.; Cooper, K. R.; White, L. A.; Häggblom, M. M. Microbially mediated O-methylation of bisphenol A results in metabolites with increased toxicity to the developing zebrafish (Danio rerio) embryo. Environ. Sci. Technol. 2011, 45 (15), 6567–6574. George, O.; Bryant, B. K.; Chinnasamy, R.; Corona, C.; Arterburn, J. B.; Shuster, C. B. Bisphenol A directly targets tubulin to disrupt spindle organization in embryonic and somatic cells. ACS Chem. Biol. 2008, 3 (3), 167–179. Lehmann, L.; Metzler, M. Bisphenol A and its methylated congeners inhibit growth and interfere with microtubules in human fibroblasts in vitro. Chem. Biol. Interact. 2004, 147 (3), 273–285. Roh, H.; Subramanya, N.; Zhao, F.; Yu, C.-P.; Sandt, J.; Chu, K.-H. Biodegradation potential of wastewater micropollutants by ammonia-oxidizing bacteria. Chemosphere 2009, 77 (8), 1084–1089. Kim, J. Y.; Ryu, K.; Kim, E. J.; Choe, W. S.; Cha, G. C.; Yoo, I.-K. Degradation of bisphenol A and nonylphenol by nitrifying activated sludge. Process Biochem. 2007, 42 (10), 1470–1474. Sun, Q.; Li, Y.; Chou, P. H.; Peng, P. Y.; Yu, C. P. Transformation of bisphenol A and alkylphenols by ammonia-oxidizing bacteria through nitration. Environ. Sci. Technol. 2012, 46 (8), 4442–4448. Holmes, A. J.; Costello, A.; Lidstrom, M. E.; Murrell, J. C. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 1995, 132, 203–208. Hanson, R. S.; Hanson, T. E. Methanotrophic bacteria. Microbiol. Rev. 1996, 60 (2), 439– 471. Im, J.; Semrau, J. D. Pollutant degradation by a Methylocystis strain SB2 grown on ethanol: Bioremediation via facultative methanotrophy. FEMS Microbiol. Lett. 2011, 318 (2), 137–142.


24


656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698

(80)

(81)

(82)

(83) (84) (85)

(86) (87) (88) (89)

(90)

(91)

(92)

(93) (94)

Page 26 of 44

Lee, S.-W.; Keeney, D. R.; Lim, D.-H.; Dispirito, A. A.; Semrau, J. D. Mixed pollutant degradation by Methylosinus trichosporium OB3b expressing either soluble or particulate methane monooxygenase: can the tortoise beat the hare? Appl. Environ. Microbiol. 2006, 72 (12), 7503–7509. Stein, L. Y.; Yoon, S.; Semrau, J. D.; DiSpirito, A. a.; Crombie, A.; Murrell, J. C.; Vuilleumier, S.; Kalyuzhnaya, M. G.; Op Den Camp, H. J. M.; Bringel, F.; et al. Genome sequence of the obligate methanotroph Methylosinus trichosporium strain OB3b. J. Bacteriol. 2010, 192 (24), 6497–6498. Telke, A. A.; Kalyani, D. C.; Jadhav, U. U.; Parshetti, G. K.; Govindwar, S. P. Purification and characterization of an extracellular laccase from a Pseudomonas sp. LBC1 and its application for the removal of bisphenol A. J. Mol. Catal. B Enzym. 2009, 61 (3-4), 252–260. Madhavi, V.; Lele, S. S. Laccase: Properties and applications. BioResources 2009, 4 (4), 1694–1717. Chai, W.; Handa, Y.; Suzuki, M.; Saito, M. Biodegradation of bisphenol A by fungi. Appl. Biochem. Biotechnol. 2005, 120 (3), 175–182. Cajthaml, T.; Křesinová, Z.; Svobodová, K.; Möder, M. Biodegradation of endocrinedisrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere 2009, 75 (6), 745–750. Karigar, C. S.; Rao, S. S. Role of microbial enzymes in the bioremediation of pollutants: A review. Enzyme Res. 2011, 2011, Article ID 805187. Husain, Q.; Qayyum, S. Biological and enzymatic treatment of bisphenol A and other endocrine disrupting compounds: A review. Crit. Rev. Biotechnol. 2013, 33 (3), 260–292. Cajthaml, T. Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Environ. Microbiol. 2015, 17 (12), 4822-4834. Hirano, T.; Honda, Y.; Watanabe, T.; Kuwahara, M. Degradation of bisphenol A by the lignin-degrading enzyme, manganese peroxidase, produced by the white-rot basidiomycete, Pleurotus ostreatus. Biosci. Biotechnol. Biochem. 2000, 64 (9), 1958– 1962. Tsutsumi, Y.; Haneda, T.; Nishida, T. Removal of estrogenic activities of bisphenol A and nonylphenol by oxidative enzymes from lignin-degrading basidiomycetes. Chemosphere 2001, 42 (3), 271–276. Nitheranont, T.; Watanabe, A.; Suzuki, T.; Katayama, T.; Asada, Y. Decolorization of synthetic dyes and biodegradation of bisphenol A by laccase from the edible mushroom, Grifola frondosa. Biosci. Biotechnol. Biochem. 2011, 75 (9), 1845–1847. Cabana, H.; Jiwan, J.-L. H.; Rozenberg, R.; Elisashvili, V.; Penninckx, M.; Agathos, S. N.; Jones, J. P. Elimination of endocrine disrupting chemicals nonylphenol and bisphenol A and personal care product ingredient triclosan using enzyme preparation from the white rot fungus Coriolopsis polyzona. Chemosphere 2007, 67 (4), 770–778. Macellaro, G.; Pezzella, C.; Cicatiello, P.; Sannia, G.; Piscitelli, A. Fungal laccases degradation of endocrine disrupting compounds. Biomed Res. Int. 2014, 2014. Uchida, H.; Fukuda, T.; Miyamoto, H.; Kawabata, T.; Suzuki, M.; Uwajima, T. Polymerization of bisphenol A by purified laccase from Trametes villosa. Biochem.


25

Page 27 of 44

699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732 733 734 735 736 737 738 739 740 741


(95)

(96) (97)

(98)

(99)

(100)

(101) (102)

(103) (104)

(105) (106)

(107) (108) (109)

(110)

Biophys. Res. Commun. 2001, 287 (2), 355–358. Tanaka, T.; Tonosaki, T.; Nose, M.; Tomidokoro, N.; Kadomura, N.; Fujii, T.; Taniguchi, M. Treatment of model soils contaminated with phenolic endocrine-disrupting chemicals with laccase from Trametes sp. in a rotating reactor. J. Biosci. Bioeng. 2001, 92 (4), 312– 316. Priyadarshani, I., Sahu, D.; Rath, B. Microalgal bioremediation: Current practices and perspectives. J. Biochem. Technol. 2012, 3 (3), 299–304. Hirooka, T.; Akiyama, Y.; Tsuji, N.; Nakamura, T.; Nagase, H.; Hirata, K.; Miyamoto, K. Removal of hazardous phenols by microalgae under photoautotrophic conditions. J. Biosci. Bioeng. 2003, 95 (2), 200–203. Ishihara, K.; Nakajima, N. Improvement of marine environmental pollution using ecosystem: Decomposition and recovery of endocrine disrupting chemicals by marine phytoand zooplanktons. J. Mol. Catal. B Enzym. 2003, 23 (2-6), 419–424. Nakajima, N.; Teramoto, T.; Kasai, F.; Sano, T.; Tamaoki, M.; Aono, M.; Kubo, A.; Kamada, H.; Azumi, Y.; Saji, H. Glycosylation of bisphenol A by freshwater microalgae. Chemosphere 2007, 69 (6), 934–941. Shimoda, K.; Hamada, H. Bioremediation of bisphenol A and benzophenone by glycosylation with immobilized marine microalga Pavlova sp. Environ. Health Insights 2009, 3, 89–94. Yim, S.-H.; Kim, H. J.; Lee, I.-S. Microbial metabolism of the environmental estrogen bisphenol A. Arch. Pharm. Res. 2003, 26 (10), 805–808. Nakajima, N. Processing of bisphenol A by plant tissues: Glucosylation by cultured BY-2 cells and glucosylation/translocation by plants of Nicotiana tabacum. Plant Cell Physiol. 2002, 43 (9), 1036–1042. Nakajima, N.; Oshima, Y.; Edmonds, J. S.; Morita, M. Glycosylation of bisphenol A by tobacco BY-2 cells. Phytochemistry 2004, 65 (10), 1383–1387. Noureddin, I. M.; Furumoto, T.; Ishida, Y.; Fukui, H. Absorption and metabolism of bisphenol A, a possible endocrine disruptor, in the aquatic edible plant, water convolvulus (Ipomoea aquatica). Biosci. Biotechnol. Biochem. 2004, 68 (6), 1398–1402. Schmidt, B.; Schuphan, I. Metabolism of the environmental estrogen bisphenol A by plant cell suspension cultures. Chemosphere 2002, 49 (1), 51–59. Gattullo, C. E.; Kiersch, K.; Eckhardt, K.-U.; Baum, C.; Leinweber, P.; Loffredo, E. Decontamination activity of ryegrass exudates towards bisphenol A in the absence and presence of dissolved natural organic matter. Int. J. Phytoremediation 2015, 17 (1), 1–8. Eio, E. J.; Kawai, M.; Niwa, C.; Ito, M.; Yamamoto, S.; Toda, T. Biodegradation of bisphenol A by an algal-bacterial system. Environ. Sci. Pollut. Res. 2015, 1–5. Salt, D. E.; Smith, R. D.; Raskin, I. Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49 (1), 643–668. Noureddin, I. M.; Furumoto, T.; Yamagishi, M.; Ishida, Y.; Fukui, H. Absorption, translocation and metabolism of bisphenol A, a possible endocrine disruptor, in rice seedlings. Environ. Control Biol. 2004, 42 (1), 31–40. Imai, S.; Shiraishi, A.; Gamo, K.; Watanabe, I.; Okuhata, H.; Miyasaka, H.; Ikeda, K.; Bamba, T.; Hirata, K. Removal of phenolic endocrine disruptors by Portulaca oleracea. J.


26


742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784

(111)

(112) (113) (114)

(115)

(116)

(117)

(118) (119) (120) (121)

(122)

(123) (124) (125)

(126) (127)

Page 28 of 44

Biosci. Bioeng. 2007, 103 (5), 420–426. Hamada, H.; Tomi, R.; Asada, Y.; Furuya, T. Phytoremediation of bisphenol A by cultured suspension cells of Eucalyptus perriniana-regioselective hydroxylation and glycosylation. Tetrahedron Lett. 2002, 43 (22), 4087–4089. Takahashi, M.; Tsukamoto, S.; Kawaguchi, A.; Sakamoto, A.; Morikawa, H. Phytoremediators from abandoned rice field. Plant Biotechnol. 2005, 22 (2), 167–170. Kang, J. H.; Kondo, F. Distribution and biodegradation of Bisphenol A in water hyacinth. Bull. Environ. Contam. Toxicol. 2006, 77 (4), 500–507. Okuhata, H.; Ikeda, K.; Miyasaka, H.; Takahashi, S.; Matsui, T.; Nakayama, H.; Kato, K.; Hirata, K. Floricultural Salvia plants have a high ability to eliminate bisphenol A. J. Biosci. Bioeng. 2010, 110 (1), 99–101. Saiyood, S.; Inthorn, D.; Vangnai, a. S.; Thiravetyan, P. Phytoremediation of Bisphenol A and total dissolved solids by the mangrove plant, Bruguiera gymnorhiza. Int. J. Phytoremediation 2013, 15 (5), 427–438. Saiyood, S.; Vangnai, a. S.; Thiravetyan, P.; Inthorn, D. Bisphenol A removal by the Dracaena plant and the role of plant-associating bacteria. J. Hazard. Mater. 2010, 178 (13), 777–785. Chai, W.; Sakamaki, H.; Kitanaka, S.; Saito, M.; Horiuchi, C. A. Biodegradation of bisphenol A by cultured cells of Caragana chamlagu. Biosci. Biotechnol. Biochem. 2003, 67 (January 2015), 218–220. Sakuyama, H.; Endo, Y.; Fujimoto, K.; Hatana, Y. Oxidative degradation of alkylphenols by horseradish peroxidase. J. Biosci. Bioeng. 2003, 96 (3), 227–231. Hong-Mei, L.; Nicell, J. A. Biocatalytic oxidation of bisphenol A in a reverse micelle system using horseradish peroxidase. Bioresour. Technol. 2008, 99 (10), 4428–4437. Xuan, Y. J.; Endo, Y.; Fujimoto, K. Oxidative degradation of bisphenol A by crude enzyme prepared from potato. J. Agric. Food Chem. 2002, 50 (22), 6575–6578. Watanabe, C.; Kashiwada, A.; Matsuda, K.; Yamada, K. Soybean peroxidase-catalyzed treatment and removal of BPA and bisphenol derivatives from aqueous solutions. Environ. Prog. Sustain. Energy 2011, 30 (1), 81–91. Huang, Q.; Weber, W. J. Transformation and removal of bisphenol A from aqueous phase via peroxidase-mediated oxidative coupling reactions: Efficacy, products, and pathways. Environ. Sci. Technol. 2005, 39 (16), 6029–6036. Kang, J.-H.; Kondo, F. Bisphenol A degradation by bacteria isolated from river water. Arch. Environ. Contam. Toxicol. 2002, 43 (3), 265–269. Kang, J.-H.; Kondo, F. Bisphenol A degradation in seawater is different from that in river water. Chemosphere 2005, 60 (9), 1288–1292. Voordeckers, J. W.; Fennell, D. E.; Jones, K.; Häggblom, M. M. Anaerobic biotransformation of tetrabromobisphenol A, tetrachlorobisphenol A, and bisphenol A in estuarine sediments. Environ. Sci. Technol. 2002, 36 (4), 696–701. Ying, G.; Kookana, R. Degradation of five selected endocrine-disrupting chemicals in seawater and marine sediment. Environ. Sci. Technol. 2003, 37 (7), 1256–1260. Bolz, U.; Hagenmaier, H.; Körner, W. Phenolic xenoestrogens in surface water, sediments, and sewage sludge from Baden-Württemberg, south-west Germany. Environ.


27

Page 29 of 44

785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827


(128) (129) (130) (131)

(132)

(133)

(134)

(135)

(136)

(137) (138)

(139)

(140) (141)

(142) (143)

Pollut. 2001, 115 (2), 291–301. Heemken, O. P.; Reincke, H.; Stachel, B.; Theobald, N. The occurrence of xenoestrogens in the Elbe river and the North Sea. Chemosphere 2001, 45 (3), 245–259. Kang, J. H.; Kondo, F. Effects of bacterial counts and temperature on the biodegradation of bisphenol A in river water. Chemosphere 2002, 49, 493–498. Ronen, Z.; Abeliovich, a. Anaerobic-aerobic process for microbial degradation of tetrabromobisphenol A. Appl. Environ. Microbiol. 2000, 66 (6), 2372–2377. Arbeli, Z.; Ronen, Z.; Drıaz-Báez, M. C. Reductive dehalogenation of tetrabromobisphenol-A by sediment from a contaminated ephemeral streambed and an enrichment culture. Chemosphere 2006, 64 (9), 1472–1478. Iasur-Kruh, L.; Ronen, Z.; Arbeli, Z.; Nejidat, A. Characterization of an enrichment culture debrominating tetrabromobisphenol A and optimization of its activity under anaerobic conditions. J. Appl. Microbiol. 2010, 109 (2), 707–715. An, T.; Zu, L.; Li, G.; Wan, S.; Mai, B.; Wong, P. K. One-step process for debromination and aerobic mineralization of tetrabromobisphenol-A by a novel Ochrobactrum sp. T isolated from an e-waste recycling site. Bioresour. Technol. 2011, 102 (19), 9148–9154. Brenner, A.; Mukmenev, I.; Abeliovich, A.; Kushmaro, A. Biodegradability of tetrabromobisphenol A and tribromophenol by activated sludge. Ecotoxicology 2006, 15 (4), 399–402. Nyholm, J. R.; Lundberg, C.; Andersson, P. L. Biodegradation kinetics of selected brominated flame retardants in aerobic and anaerobic soil. Environ. Pollut. 2010, 158 (6), 2235–2240. Patterson, B. M.; Shackleton, M.; Furness, A. J.; Pearce, J.; Descourvieres, C.; Linge, K. L.; Busetti, F.; Spadek, T. Fate of nine recycled water trace organic contaminants and metal(loid)s during managed aquifer recharge into a anaerobic aquifer: Column studies. Water Res. 2010, 44 (5), 1471–1481. Sarmah, A. K.; Northcott, G. L. Laboratory degradation studies of four endocrine disruptors in two environmental media. Environ. Toxicol. Chem. 2008, 27 (4), 819–827. Li, G.; Zu, L.; Wong, P.-K.; Hui, X.; Lu, Y.; Xiong, J.; An, T. Biodegradation and detoxification of bisphenol A with one newly-isolated strain Bacillus sp. GZB: Kinetics, mechanism and estrogenic transition. Bioresour. Technol. 2012, 114, 224–230. Endo, Y.; Kimura, N.; Ikeda, I.; Fujimoto, K.; Kimoto, H. Adsorption of bisphenol A by lactic acid bacteria, Lactococcus strains. Appl. Microbiol. Biotechnol. 2007, 74 (1), 202– 207. Im, J.; Yip, D.; Lee, J.; Löffler, F. E. Simplified extraction of bisphenols from bacterial culture suspensions and solid matrices. J. Microbiol. Methods 2016, 126, 35–37. Balmer, M. E.; Goss, K. U.; Schwarzenbach, R. P. Photolytic transformation of organic pollutants on soil surfaces - An experimental approach. Environ. Sci. Technol. 2000, 34 (7), 1240–1245. Dabrowska, D.; Kot-Wasik, A.; Namieśnik, J. Pathways and analytical tools in degradation studies of organic pollutants. Crit. Rev. Anal. Chem. 2005, 35 (2), 155–176. Howard, P. H. Handbook of environmental fate and exposure data: For organic chemicals Vol 1; Lewis Publishers: Chelsea, MI, 1989.


28


828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866 867 868 869 870

Page 30 of 44

(144) Mack, J.; Bolton, J. R. Photochemistry of nitrite and nitrate in aqueous solution: A review. J. Photochem. Photobiol. A Chem. 1999, 128 (1-3), 1–13. (145) Peng, Z.; Wu, F.; Deng, N. Photodegradation of bisphenol A in simulated lake water containing algae, humic acid and ferric ions. Environ. Pollut. 2006, 144 (3), 840–846. (146) Zhan, M. J.; Yang, X.; Xian, Q. M.; Kong, L. R. Photochemical transformation of bisphenol A promoted by nitrate ions. Bull. Environ. Contam. Toxicol. 2006, 76 (1), 105– 112. (147) Chin, Y. P.; Miller, P. L.; Zeng, L.; Cawley, K.; Weavers, L. K. Photosensitized degradation of bisphenol A by dissolved organic matter. Environ. Sci. Technol. 2004, 38 (22), 5888–5894. (148) Zhang, C. X.; Wang, Y. X. Effects of dissolved organic matter in landfill leachate on photodegradation of environmental endocrine disruptors. Int. J. Environ. Pollut. 2011, 45 (1/2/3), 69. (149) Zhou, D.; Wu, F.; Deng, N.; Xiang, W. Photooxidation of bisphenol A (BPA) in water in the presence of ferric and carboxylate salts. Water Res. 2004, 38 (19), 4107–4116. (150) Sajiki, J.; Yonekubo, J. Degradation of bisphenol-A (BPA) in the presence of reactive oxygen species and its acceleration by lipids and sodium chloride. Chemosphere 2002, 46 (2), 345–354. (151) Barbieri, Y.; Massad, W. A.; Díaz, D. J.; Sanz, J.; Amat-Guerri, F.; García, N. A. Photodegradation of bisphenol A and related compounds under natural-like conditions in the presence of riboflavin: Kinetics, mechanism and photoproducts. Chemosphere 2008, 73 (4), 564–571. (152) Ha, D. O.; Jeong, M. K.; Park, C. U.; Park, M. H.; Chang, P. S.; Lee, J. H. Effects of riboflavin photosensitization on the degradation of bisphenol A (BPA) in model and realfood systems. J. Food Sci. 2009, 74 (5), 380–384. (153) Liu, Z. hua; Kanjo, Y.; Mizutani, S. Removal mechanisms for endocrine disrupting compounds (EDCs) in wastewater treatment - physical means, biodegradation, and chemical advanced oxidation: A review. Sci. Total Environ. 2009, 407 (2), 731–748. (154) Arslan-Alaton, I.; Olmez-Hanci, T. Advanced oxidation of endocrine disrupting compounds: Review on photo-fenton treatment of alkylphenols and bisphenol A; 2012; pp 59–90. (155) Cesaro, A.; Belgiorno, V. Removal of endocrine disruptors from urban wastewater by advanced oxidation processes (AOPs): A review. Open Biotechnol. J. 2016, 10 (Suppl-1, M12), 151–172. (156) Belgiorno, V.; Rizzo, L.; Fatta, D.; Della Rocca, C.; Lofrano, G.; Nikolaou, A.; Naddeo, V.; Meric, S. Review on endocrine disrupting-emerging compounds in urban wastewater: occurrence and removal by photocatalysis and ultrasonic irradiation for wastewater reuse. Desalination 2007, 215 (1-3), 166–176. (157) Gültekin, I.; Ince, N. H. Synthetic endocrine disruptors in the environment and water remediation by advanced oxidation processes. J. Environ. Manage. 2007, 85 (4), 816–832. (158) Sekar, R.; Dichristina, T. J. Microbially driven fenton reaction for degradation of the widespread environmental contaminant 1,4-dioxane. Environ. Sci. Technol. 2014, 48 (21), 12858–12867.


29

Page 31 of 44

871 872 873 874 875 876 877 878 879 880 881 882 883 884 885 886 887 888 889 890 891 892 893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913


(159) Raychoudhury, T.; Scheytt, T. Potential of zerovalent iron nanoparticles for remediation of environmental organic contaminants in water: A review. Water Sci. Technol. 2013, 68 (7), 1425–1439. (160) Clark, C. J.; Cooper, A. T.; Martin, C. L.; Pipkin, L. Evaluation of potential degradation of bisphenol A by zero-valent iron (ZVI). Environ. Forensics 2012, 13 (3), 248–254. (161) Girit, B.; Dursun, D.; Olmez-Hanci, T.; Arslan-Alaton, I. Treatment of aqueous bisphenol A using nano-sized zero-valent iron in the presence of hydrogen peroxide and persulfate oxidants. Water Sci. Technol. 2015, 71 (12), 1859. (162) Stone, A. Reductive dissolution of manganese(III/IV) oxides by substituted phenols. Environ. Sci. Technol. 1987, 21 (10), 979–988. (163) Cheney, M. A.; Shin, J. Y.; Crowley, D. E.; Alvey, S.; Malengreau, N.; Sposito, G. Atrazine dealkylation on a manganese oxide surface. Colloids Surfaces A Physicochem. Eng. Asp. 1998, 137 (1-3), 267–273. (164) Learman, D. R.; Voelker, B. M.; Vazquez-Rodriguez, A. I.; Hansel, C. M. Formation of manganese oxides by bacterially generated superoxide. Nat. Geosci. 2011, 4 (2), 95–98. (165) Lin, K.; Liu, W.; Gant, J. Oxidative removal of bisphenol A by manganese dioxide: Efficacy, products, and pathways. Environ. Sci. Technol. 2009, 43 (10), 3860–3864. (166) Lin, K.; Peng, Y.; Huang, X.; Ding, J. Transformation of bisphenol A by manganese oxide-coated sand. Environ. Sci. Pollut. Res. Int. 2013, 20 (3), 1461–1467. (167) Gao, N.; Hong, J.; Yu, Z.; Peng, P.; Huang, W. Transformation of bisphenol A in the presence of manganese dioxide. Soil Sci. 2011, 176 (6), 265–272. (168) Im, J.; Prevatte, C. W.; Campagna, S. R.; Löffler, F. E. Identification of 4-hydroxycumyl alcohol as the major MnO2-mediated Bisphenol A transformation product and evaluation of its environmental fate. Environ. Sci. Technol. 2015, 49 (10), 6214–6221. (169) Klausen, J.; Haderlein, S. B.; Schwarzenbach, R. P. Oxidation of substituted anilines by aqueous MnO2 : Effect of co-solutes on initial and quasi-steady-state kinetics. Environ. Sci. Technol. 1997, 31 (9), 2642–2649. (170) Tebo, B. M.; Bargar, J. R.; Clement, B. G.; Dick, G. J.; Murray, K. J.; Parker, D.; Verity, R.; Webb, S. M. Biogenic manganese oxides: Properties and mechanisms of formation. Annu. Rev. Earth Planet. Sci. 2004, 32 (1), 287–328. (171) Li, F.; Liu, C.; Liang, C.; Li, X.; Zhang, L. The oxidative degradation of 2mercaptobenzothiazole at the interface of b-MnO2 and water. J. Hazard. Mater. 2008, 154 (1-3), 1098–1105. (172) Grebel, J. E.; Charbonnet, J. A.; Sedlak, D. L. Oxidation of organic contaminants by manganese oxide geomedia for passive urban stormwater treatment systems. Water Res. 2016, 88, 481–491. (173) Amonette, J. E.; Workman, D. J.; Kennedy, D. W.; Fruchter, J. S.; Gorby, Y. A. Dechlorination of carbon tetrachloride by Fe(II) associated with goethite. Environ. Sci. Technol. 2000, 34 (21), 4606–4613. (174) Klupinski, T. P.; Chin, Y.-P.; Traina, S. J. Abiotic degradation of pentachloronitrobenzene by Fe(II): Reactions on goethite and iron oxide nanoparticles. Environ. Sci. Technol. 2004, 38 (16), 4353–4360. (175) Lin, K.; Ding, J.; Wang, H.; Huang, X.; Gan, J. Goethite-mediated transformation of


30


914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956

(176) (177)

(178) (179)

(180) (181) (182)

(183) (184)

(185)

(186)

(187) (188)

(189) (190)

(191)

(192)

Page 32 of 44

bisphenol A. Chemosphere 2012, 89 (7), 789–795. Huang, P. M.; Li, Y.; Sumner, M. E. Handbook of soil sciences: Properties and processes; Handbook of Soil Science; CRC Press, 2011. Vandieken, V.; Pester, M.; Finke, N.; Hyun, J.-H.; Friedrich, M. W.; Loy, A.; Thamdrup, B. Three manganese oxide-rich marine sediments harbor similar communities of acetateoxidizing manganese-reducing bacteria. ISME J. 2012, 6 (11), 2078–2090. Sigg, L.; Sturm, M.; Kistler, D. Vertical transport of heavy metals by settling particles in Lake Zurich. Limnol. Oceanogr. 1987, 32 (l), 112–130. Kepay, P. E. Kinetics of microbial manganese oxidation and trace metal binding in sediments: Results from an in situ dialysis technique. Limnol. Oceanogr. 1985, 30 (4), 713–726. Zhang, H.; Huang, C.-H. Oxidative transformation of triclosan and chlorophene by manganese oxides. Environ. Sci. Technol. 2003, 37 (11), 2421–2430. Remucal, C. K.; Ginder-Vogel, M. A critical review of the reactivity of manganese oxides with organic contaminants. Environ. Sci. Process. Impacts 2014, 16 (6), 1247–1266. Lafferty, B. J.; Ginder-Vogel, M.; Sparks, D. L. Arsenite oxidation by a poorly crystalline manganese-oxide 1. Stirred-flow experiments. Environ. Sci. Technol. 2010, 44 (22), 8460–8466. Verstraete, W.; Devliegher, W. Formation of non-bioavailable organic residues in soil: Perspectives for site remediation. Biodegradation 1997, 7 (6), 471–485. Kearney, P. C. Summary of Soil Bound Residues Discussion Session. In ACS Symposium Series; Kaufman, D.D.,. Still, G.G., Paulson, G.D., Bandal, S. K., Ed.; ACS: Washington, 1976; pp 378–382. Kästner, M.; Streibich, S.; Beyrer, M.; Richnow, H. H.; Fritsche, W. Formation of bound residues during microbial degradation of 14C anthracene in soil. Appl. Environ. Microbiol. 1999, 65 (5), 1834–1842. Barriuso, E.; Benoit, P.; Dubus, I. G. Formation of pesticide nonextractable (bound) residues in soil: Magnitude, controlling factors and reversibility. Environ. Sci. Technol. 2008, 42 (6), 1845–1854. Gevao, B.; Semple, K. T.; Jones, K. C. Bound pesticide residues in soils: A review. Environ. Pollut. 2000, 108 (1), 3–14. Coates, J. D.; Chakraborty, R.; O’Connor, S. M.; Schmidt, C.; Thieme, J. The geochemical effects of microbial humic substances reduction. Acta Hydrochim. Hydrobiol. 2001, 28 (7), 420–427. Hsu, T.-S.; Bartha, R. Interaction of pesticide-derived chloroaniline residues with soil organic matter. Soil Sci. 1973, 116 (6), 444–452. Klečka, G. M.; Staples, C. A.; Clark, K. E.; van der Hoeven, N.; Thomas, D. E.; Hentges, S. G. Exposure analysis of bisphenol A in surface water systems in North America and Europe. Environ. Sci. Technol. 2009, 43 (16), 6145–6150. Staples, C.; Mihaich, E.; Ortego, L.; Caspers, N.; Klečka, G.; Woelz, J.; Hentges, S. Characterizing the effects of bisphenol A on sediment dwelling benthic organisms. Environ. Toxicol. Chem. 2015, 35 (3), n/a – n/a. Kolpin, D. W.; Furlong, E. T.; Meyer, M. T.; Thurman, E. M.; Zaugg, S. D.; Barber, L.


31

Page 33 of 44

957 958 959 960 961 962 963 964 965 966 967 968 969 970 971 972 973 974 975 976 977 978 979 980 981 982 983 984 985 986 987 988 989 990 991 992 993 994 995 996 997 998 999


(193) (194)

(195)

(196)

(197)

(198) (199) (200) (201)

(202)

(203)

(204)

(205) (206)

(207)

B.; Buxton, H. T. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: A national reconnaissance. Environ. Sci. Technol. 2002, 36 (6), 1202–1211. Michalowicz, J. Bisphenol A - Sources, toxicity and biotransformation. Environ. Toxicol. Pharmacol. 2014, 37 (2), 738–758. Corrales, J.; Kristofco, L. a.; Steele, W. B.; Yates, B. S.; Breed, C. S.; Williams, E. S.; Brooks, B. W. Global assessment of bisphenol A in the environment: Review and analysis of its occurrence and bioaccumulation. Dose-Response 2015, 13 (3), 1–29. Careghini, A.; Mastorgio, A. F.; Saponaro, S.; Sezenna, E. Bisphenol A, nonylphenols, benzophenones, and benzotriazoles in soils, groundwater, surface water, sediments, and food: a review. Environ. Sci. Pollut. Res. 2015, 22 (8), 5711–5741. Huang, D. Y.; Zhao, H. Q.; Liu, C. P.; Sun, C. X. Characteristics, sources, and transport of tetrabromobisphenol A and bisphenol A in soils from a typical e-waste recycling area in South China. Environ. Sci. Pollut. Res. 2014, 21, 5818–5826. Dulio, V.; Slobodnik, J. NORMAN-network of reference laboratories, research centres and related organisations for monitoring of emerging substances. Environ. Sci. Pollut. Res. 2009, 16 (SUPPL1), 132–135. Chang, B. V.; Yuan, S. Y.; Chiou, C. C. Biodegradation of bisphenol-A in river sediment. J. Environ. Sci. Heal. Part A 2011, 46 (9), 931–937. Tanghe, T.; Dhooge, W.; Verstraete, W. Isolation of a bacterial strain able to degrade branched nonylphenol. Appl. Environ. Microbiol. 1999, 65 (2), 746–751. Hu, A.; Lv, M.; Yu, C.-P. Draft genome sequence of the bisphenol A-degrading bacterium Sphingobium sp. strain YL23. Genome Announc. 2013, 1 (4), e00549–13 – e00549–13. Li, Y.; Toyama, T.; Furuya, T.; Iwanaga, K.; Tanaka, Y.; Mori, K. Sustainable biodegradation of Bisphenol A by Spirodela polyrhiza in association with Novosphingobium sp. FID3. J. Water Environ. Technol. 2014, 12 (1), 43–54. Zhang, C.; Zeng, G.; Yuan, L.; Yu, J.; Li, J.; Huang, G.; Xi, B.; Liu, H. Aerobic degradation of bisphenol A by Achromobacter xylosoxidans strain B-16 isolated from compost leachate of municipal solid waste. Chemosphere 2007, 68 (1), 181–190. Mita, L.; Grumiro, L.; Rossi, S.; Bianco, C.; Defez, R.; Gallo, P.; Mita, D. G.; Diano, N. Bisphenol A removal by a Pseudomonas aeruginosa immobilized on granular activated carbon and operating in a fluidized bed reactor. J. Hazard. Mater. 2015, 291, 129–135. Badiefar, L.; Yakhchali, B.; Rodriguez-Couto, S.; Veloso, A.; García-Arenzana, J. M.; Matsumura, Y.; Khodabandeh, M. Biodegradation of bisphenol A by the newly-isolated Enterobacter gergoviae strain BYK-7 enhanced using genetic manipulation. RSC Adv. 2015, 5 (37), 29563–29572. Gulnaz, O.; Dincer, S. Biodegradation of bisphenol A by Chlorella vulgaris and Aeromonas Hydrophilia. J. Appl. Biol. Sci. 2009, 3 (2), 79–84. Masuda, M.; Yamasaki, Y.; Ueno, S.; Inoue, A. Isolation of bisphenol Atolerant/degrading Pseudomonas monteilii strain N-502. Extremophiles 2007, 11 (2), 355– 362. Peng, Y. H.; Chen, Y. J.; Chang, Y. J.; Shih, Y. hsin. Biodegradation of bisphenol A with diverse microorganisms from river sediment. J. Hazard. Mater. 2015, 286, 285–290.


32


1000 1001 1002 1003 1004 1005 1006 1007 1008 1009 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020 1021 1022 1023 1024 1025 1026 1027 1028 1029 1030 1031 1032 1033 1034 1035 1036 1037 1038 1039 1040 1041 1042

Page 34 of 44

(208) Liu, F.; Liu, Q.; Zhang, Y.; Liu, Y.; Wan, Y.; Gao, K.; Huang, Y.; Xia, W.; Wang, H.; Shi, Y.; et al. Molecularly imprinted nanofiber membranes enhanced biodegradation of trace bisphenol A by Pseudomonas aeruginosa. Chem. Eng. J. 2015, 262, 989–998. (209) Kamaraj, M.; Sivaraj, R.; Venckatesh, R. Biodegradation of Bisphenol A by the tolerant bacterial species isolated from coastal regions of Chennai, Tamil Nadu, India. Int. Biodeterior. Biodegradation 2014, 93, 216–222. (210) Zühlke, M.-K.; Schlüter, R.; Henning, A.-K.; Lipka, M.; Mikolasch, A.; Schumann, P.; Giersberg, M.; Kunze, G.; Schauer, F. A novel mechanism of conjugate formation of bisphenol A and its analogues by Bacillus amyloliquefaciens: Detoxification and reduction of estrogenicity of bisphenols. Int. Biodeterior. Biodegradation 2016, 109, 165–173. (211) Yamanaka, H.; Moriyoshi, K.; Ohmoto, T.; Ohe, T.; Sakai, K. Degradation of bisphenol a by Bacillus pumilus isolated from kimchi, a traditionally fermented food. Appl. Biochem. Biotechnol. 2007, 136, 39–51. (212) Kang, J.-H.; Ri, N.; Kondo, F. Streptomyces sp. strain isolated from river water has high bisphenol A degradability. Lett. Appl. Microbiol. 2004, 39 (2), 178–180. (213) Ren, L.; Jia, Y.; Ruth, N.; Shi, Y.; Wang, J.; Qiao, C.; Yan, Y. Biotransformations of bisphenols mediated by a novel Arthrobacter sp. strain YC-RL1. Appl. Microbiol. Biotechnol. 2015. (214) Shin, E. H.; Choi, H. T.; Song, H. G. Biodegradation of endocrine-disrupting bisphenol A by white rot fungus Irpex lacteus. J. Microbiol. Biotechnol. 2007, 17, 1147–1151. (215) Kim, Y.; Yeo, S.; Song, H. G.; Choi, H. T. Enhanced expression of laccase during the degradation of endocrine disrupting chemicals in Trametes versicolor. J. Microbiol. 2008, 46 (4), 402–407. (216) Sakurai, A.; Toyoda, S.; Sakakibara, M. Removal of bisphenol A by polymerization and precipitation method using Coprinus cinereus peroxidase. Biotechnol. Lett. 2001, 23 (12), 995–998. (217) Eibes, G.; Debernardi, G.; Feijoo, G.; Moreira, M. T.; Lema, J. M. Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation 2011, 22, 539–550. (218) Fukuda, T.; Uchida, H.; Takashima, Y.; Uwajima, T.; Kawabata, T.; Suzuki, M. Degradation of bisphenol A by purified laccase from Trametes villosa. Biochem. Biophys. Res. Commun. 2001, 284 (3), 704–706. (219) Tanaka, T.; Yamada, K.; Tonosaki, T.; Konishi, T.; Goto, H.; Taniguchi, M. Enzymatic degradation of alkylphenols, bisphenol A, synthetic estrogen and phthalic ester. Water Sci. Technol. 2000, 42, 89–95. (220) Gassara, F.; Brar, S. K.; Verma, M.; Tyagi, R. D. Bisphenol A degradation in water by ligninolytic enzymes. Chemosphere 2013, 92 (10), 1356–1360. (221) Asadgol, Z.; Forootanfar, H.; Rezaei, S.; Mahvi, A. H.; Faramarzi, M. A. Removal of phenol and bisphenol-A catalyzed by laccase in aqueous solution. J. Environ. Heal. Sci. Eng. 2014, 12 (1), 1–5. (222) Kum, H.; Lee, S.; Ryu, S.; Choi, H. T. Degradation of endocrine disrupting chemicals by genetic transformants with two lignin degrading enzymes in Phlebia tremellosa. J. Microbiol. 2011, 49 (5), 824–827.


33

Page 35 of 44


1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1054 1055 1056 1057 1058 1059 1060

(223) Kim, Y.; Yeo, S.; Kim, M. K.; Choi, H. T. Removal of estrogenic activity from endocrinedisrupting chemicals by purified laccase of Phlebia tremellosa. FEMS Microbiol. Lett. 2008, 284 (2), 172–175. (224) Keum, Y. S.; Lee, H. R.; Park, H. W.; Kim, J.-H. Biodegradation of bisphenol A and its halogenated analogues by Cunninghamella elegans ATCC36112. Biodegradation 2010, 21 (6), 989–997. (225) Subramanian, V.; Yadav, J. S. Role of P450 monooxygenases in the degradation of the endocrine-disrupting chemical nonylphenol by the white rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 2009, 75 (17), 5570–5580. (226) Yoshida, M.; Ono, H.; Mori, Y.; Chuda, Y.; Mori, M. Oxygenation of bisphenol A to quinones by polyphenol oxidase in vegetables. J. Agric. Food Chem. 2002, 50 (15), 4377– 4381. (227) Chang, B.-V.; Liu, J.-H.; Liao, C.-S. Aerobic degradation of bisphenol-A and its derivatives in river sediment. Environ. Technol. 2014, 35 (4), 416–424. (228) Tamura, K.; Dudley, J.; Nei, M.; Kumar, S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24 (8), 1596–1599.


34


Page 36 of 44

1061 1062 1063

Table 1. Occurrence of BPA in the environment exemplified by representative published information. Extensive compilations detailing BPA occurrence in environmental systems are publicly available (e.g., refs 10, 192, 194–197 and NORMAN-EMPODATa).

1064

Source

Concentration (ng L-1)

References

Surface water

0 – 272

127

9 – 776

128

0.5 – 410

8

140 Seawater

b

192

81b (North America), 10b (Europe)

190

0 – 249

128

b

Sewage effluent

Sewage sludge

Soil/sediment

c

Landfill leachate

b

0 (North America), 1.6 (Europe)

190

0 – 2.6

9

31 – 223

7

18 – 702

8

0 – 32.4

9

0 – 17,300 (0 – 1,500)b

10

0 – 12,500

7

70 – 770

127

4 – 1,363

8

0 – 15

127

66 – 343

128

0.01 – 0.19

8

0.6/3.5b,d (North America), 16/8.5b,d (Europe)

190

0.5 – 325

196

1.3 - 17,200 6

4.2 × 10 – 25 × 10 17,000

11 6

a

13

10 – 107,000

1065 1066 1067 1068 1069

12 14

a

NORMAN-EMPODAT Database (http://www.normandata.eu/empodat/).197 NORMAN is a network of reference laboratories, research centers and related organizations for monitoring of emerging substances. EMPODAT is a database of geo-referenced monitoring and bio-monitoring data on emerging substances in the following matrices: water, sediment, biota, soil, sewage sludge and air. bmedian value; cunit: ng g-1 d dw ; values obtained from freshwater and marine sediments, respectively;


35

Page 37 of 44

1070


Table 2. Bacterial isolates capable of degrading BPA under oxic conditions and their origins. Bacterial isolates

Origin

a-Proteobacteria

Ensifer adhaerens strain J3 Sphingomonas bisphenolicum strains AO1, Sphingomonas sp. strains MV1, AO1, SO11, BP7, and TTNP3 Sphingobium yanoikuyae strain BP-11R and Sphingobium sp. strains BiD32 and YL23 Novosphingobium sp. strains FID3, TYA-1 Sphingopyxis sp. strain BiD10 Ochrobactrum sp. strain T Alcaligenes sp. strain OIT7 Bordetella sp. strain OS17 Achromobacter xylosoxidans strain B-16 Nitrosomonas europaea Pandoraea sp. strain HYO6 Cupriavidus basilensis strain JF1 Variovorax sp. strain HCA

FW SS, WTP, SW

198 42, 47, 53, 56, 57, 199

FW, WTP SS WTP EW SS SS CL SS SS WPT SS

50, 52, 200 51, 201 52 133 56 56 202 74 56 65

Serratia rubidae strain LCA3 and Serratia sp. strain HI10 Enterobacter gergoviae strain BYK-7, Enterobacter sp. HI9, HA18, BPR1, and BPW5 Klebsiella pneumoniae strain BYK-9, Klebsiella sp. NE2, SU3 and SU5 Aeromonas hydrophila Pseudomonas monteilii strain N-502, Pseudomonas paucimobilis strain FJ-4, Pseudomonas knackmussii strain B13, Pseudomonas putida strain KA5, Pseudomonas aeruginosa strains LCS1 and 2, Pseudomonas sp. strains LBC1, KA4, SU1, SU4, SU19, KU1, and KU2 Bacillus cereus strain BPW4, Bacillus amyloliquefaciens strain Bak15a, Bacillus sp. strains BP-2CK, BP-21DK, GZB, NO13, NO15, YA27, and KU3 Streptomyces sp. Mycobacterium vanbaalenii strain PYR-1 Arthrobacter sp. strain YC-RL1

SS, FW SS, WTP SS, WTP SS SS, WTP, SW, FW, UI

56, 203 56, 116, 204 56, 204 205 56, 59, 82, 123, 203, 206, 207, 208, 209

SS, WTP, SW, FF FW FW SS

56, 107, 138, 209–211

b-Proteobacteria

g-Proteobacteria

Bacillus Actinobacteria

1071 1072

a

Classes

References

b

212 71 213

a

SS: soil/sediment; WTP: wastewater treatment plant; SW: seawater; FW: freshwater; EW: electric waste recycling site; CL: compost leachate; UI: unidentified; FF: fermented food; bIm et al., unpublished.


36


1073 1074

Page 38 of 44

Table 3. Organisms harboring enzyme systems that catalyze BPA transformation reactions. Kingdom

Species

Enzyme

References

Bacteria

Sphingomonas sp.

Cytochrome P450

53, 54, 63

Sphingobium sp.

p-hydroxybenzoate hydroxylase

68

Pseudomonas sp.

Laccase

82

Nitrosomonas europaea

Ammonia monooxygenase

74

Pleurotus ostreatus, Phanerochaete chrysosporium, Trametes versicolor, Irpex lacteus

Manganese peroxidase

89, 90, 214, 215

Coprinus cinereus, Bjerkandera adusta

Peroxidase

216, 217

Trametes vasocolor, Trametes villosa, Phanerochaete chrysosporium, Irpex lacteus, Coriolopsis polyzona, Paraconiothyrium variabile, Grifola frondosa, Phlebia tremellosa, Aspergillus niger, Phlebia tremellosa

Laccase

94–97, 214, 215, 218– 223

Cunninghamella elegans, Phanerochaete chrysosporium

Cytochrome P450

224, 225

Unspecified fungus

Polyphenol oxidase

226

Horseradish, Soy bean

Peroxidase

118, 119, 121, 122

Potato

Polyphenol oxidases

120

Fungi

Plantae


37

Page 39 of 44

1075


Table 4. BPA degradation/transformation pathways and reported kinetics constants. Degradation/transformation mechanism Bacteriaa Achromobacter xylosoxidans Alcaligenes sp. Bacillus cereus Bacillus pumilus Bacillus sp. Bordetella sp. Cupriavidus basilensis Ensifer adhaerens Enterobacter gergoviae Enterobacter sp. Klebsiella pneumonia Klebsiella sp. Novosphingobium sp. Pandoraea sp. Pseudomonas aeruginosa Pseudomonas knackmussii Pseudomonas monteilii Pseudomonas putida Pseudomonas stutzeri Pseudomonas sp. Serratia sp. Sinorhizobium fredii Sphingobium sp. Sphingomonas bisphenolicum Sphingomonas yanoikuyae Sphingomonas sp. Sphingopyxis sp. Streptomyces sp. Fungia Bjerkandera adusta Dichomitus squalens Irpex lacteus Phanerochaete chrysosporium Phanerochaete magnolia Pleurotus ostreatus Pycnoporus cinnabarinus Trametes versicolor

Initial BPA concentration (mg L-1)

First order rate constant (d-1)

Reference

3 – 10 0.3 11 10 – 50 5 – 30 250 – 1,000 0.3 0.3 0.137 250 200 11 0.3 200 0.3 114 0.23 – 1.14 0.3 0.05 10 100 – 1,000 250 250 0.3 250 – 1,000 50 0.3 250 1 60 100 300 100 1 1

0.05 – 0.01b 0.4 0.05 11.4 – 0.01b 0.7 – 0.3b 0.2 – 0.1b 0.4 – 1 0.3 0.005 1.2 0.05 – 0.2 0.1 – 0.2 0.5 – 0.6 0.1 0.2 – 0.4 11.5 4.9 – 6.3 0.4 0.1 – 1.1 0.08 – 1.1 82.9 – 9.1b 1.3 1.5 0.04 – 0.4 0.3 – 0.1b 0.8 – 2.1 0.4 0.8 4.1 7.1 0.1 2.9 0.1 – 1.2 4.3 0.3

202 56 116 211 138 209 56 56 65 198 204 116 56 204 56 201 51 56 208 207 206 198 198 56 209 227 56 198 52 200 55 50 57 52 212

10 10 10 10 10 10 90.9 10 10

0.5 0.2 0.6 0.2 0.2 0.2 0.1 0.03 0.2

85 85 85 85 85 85 89 85 85

9.1 2

0.4 0.2

97 99

c

Algae Chlorella fusca Scenedesmus acutus


38


Page 40 of 44

c

Plantae Caragana chamlagu Eichhornia crassipes Ipomoea aquatica Portulaca oleracea Oryza sativa Rumex crispus Photo-degradation simulated lake water NO3--induced degradation Reactive mineral MnO2 a-FeOOH ZVI

d

97 10 5 11.4 11.4 5.5 40

3.5 d 6.9 d 1.0 d 3.5 d 6.9 d 1.4 d 0.5

117 113 104 110 114 109 112

2 10

2.8 e 1.2 – 30.5

145 146

10 1 60 2

144 – 1,411 22g 1.6h 0.2i

f

168 165 175 160

1076

a

1077

b

1078

c

1079

(k) were calculated assuming pseudo first order kinetics using the following equation: k = – ln(A/A0) / t;

1080

d

1081

e

1082

f

1083

g

[MnO2] = 70 mg L-1 (nominal concentration at pH 7.5). Extrapolated from data shown in Figure 2 of reference 165;

1084

h

[a-FeOOH ] = 100 g L-1 (nominal concentration);

1085

i

Studies performed using purified enzymes are not included; Rate constants decreased with increasing BPA concentrations;

BPA removal occurred by a combination of adsorption and transformation. For comparison purposes, rate constants

When A = 0, A/A0 was assumed to be 0.001;

[NO3-] = 0.16 – 9.6 mM;

[MnO2] = 17.4 – 174 mg L-1 (nominal concentration at pH 7);

[ZVI] = 250 g L-1 (nominal concentration)

1086


39

Page 41 of 44


1087

1088 1089 1090

Figure 1. Major BPA sources (red), sinks and natural attenuation processes in the environment.

1091

AMO: ammonia monooxygenase, HCA: 4-hydroxycumyl alcohol, ROS: reactive oxygen

1092

species, WWTP: wastewater treatment plant.

1093


40


Page 42 of 44

1094 1095 1096

Figure 2. Summary of known pathways and intermediates of BPA degradation/transformation

1097

processes mediated by bacteria, fungi, plants and reactive mineral phases demonstrated in the

1098

laboratory. Only the major intermediates are shown and several other, presumably minor

1099

intermediates that have been reported, are not depicted. IPP: 4-isopropenylphenol; HBAL: 4-

1100

hydroxybenzaldehyde; HBA: 4-hydroxybenzoate; HAP: 4-hydroxyacetophenone; HCA: 4-

1101

hydroxycumyl alcohol; HQ: hydroquinone; MME/DME: monomethyl/dimethyl ether.


41

Page 43 of 44


Figure1 167x98mm (144 x 144 DPI)



Figure2 633x456mm (72 x 72 DPI)


Page 44 of 44

Fate of Bisphenol A in Terrestrial and Aquatic ... - ACS Publications

Recommend Documents